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Description
The goal of the Journal of Developmental Processes is to provide a vehicle for
research and clinical studies that advance knowledge of the complexity inherent in all
developmental processes. The JDP encourages exchange of ideas across fields including,
but not limited to, animal behavior, anthropology, biology, education, linguistics, neuro-
science, occupational and speech and language therapy, primatology, psychiatry, psychol-
ogy, public policy, sociology, and social work.
The Journal is interested in both experimental and descriptive studies, including
basic research, detailed case reports, ethnographic analysis, and theoretical explorations.
Particularly welcome are innovative conceptual frameworks and methods that capture the
complexity of developmental processes as well as assessment procedures and interven-
tions that enable children and families to overcome mental health, developmental, social,
and learning challenges.
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References
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style, e.g.,
please visit www.icdl.com
Greenspan, S. I., & Shanker, S. G. (2004). The first idea: How symbols, language, and or call 301-656-2667 for information
intelligence evolved from our primate ancestors to modern humans. Cambridge,
MA: Da Capo.
Greenspan, S. I., & Shanker, S. G. (2005). Developmental Research. In E. S. Person,
A. M. Cooper, & G. O. Gabbard, American psychiatric publishing textbook of psy-
choanalysis (pp. 335–360). Washington, DC: American Psychiatric Publishing.
Greenspan, S. I., & Wieder, S. (1997). Developmental patterns and outcomes in infant and
children with disorders in relating and communicating: A chart review of 200
cases of children with autistic spectrum diagnosis. Journal of Developmental and
Learning Disorders, 1, 87–141.
THE JOURNAL OF DEVELOPMENTAL PROCESSES
Volume 1 2006
CONTENTS
The Journal gratefully acknowledges the financial support of the Milton and Ethel Harris Research
Initiative (MEHRI), York University, Toronto, Canada. For more information, please see
www.MEHRI.ca
Introductory Notes
Stanley I. Greenspan, MD
Editor in Chief
Interdisciplinary Council for Developmental Learning Disorders
Department of Psychiatry, Behavioral Sciences, and Pediatrics
George Washington University Medical School
Washington, DC
The Journal of Developmental and Learning Disorders has expanded its focus and be-
come the Journal of Developmental Processes (JDP). The Editor, Barbara J. King,
Professor of Anthropology at The College of William and Mary, embodies the spirit
of the Journal in her own outstanding work, and beautifully describes it in the edito-
rial that follows. The expanded editorial board and sponsoring organizations—the
Council of Human Development, the Milton and Ethel Harris Research Initiative, in
addition to the Interdisciplinary Council on Developmental and Learning Disorders—
reflect the broad focus of the Journal. As will readily be seen, the JDP includes all the
disciplines that contribute to our understanding of human development, the factors
that influence it, the mechanisms through which they work, and the enormous varia-
tions observed throughout the course of life. The Journal embraces clinical studies
and case descriptions in keeping with the traditions established by its predecessor, the
Journal of Developmental and Learning Disorders. It also, however, focuses on a
broad range of studies and narratives that are necessary for a full understanding of de-
velopmental processes. I want to welcome you to our new Journal and hope that you
will not only enjoy reading it, but will also become part of the growing group of col-
leagues that are actively contributing to our understanding of the full complexity of
human experience.
1
A Welcome, and an Invitation, from the Editor
3
4 BARBARA J. KING
Alan Fogel
Department of Psychology
University of Utah
alan.fogel@psych.utah.edu
Abstract: This paper presents a dynamic systems methodology for the study of interindi-
vidual communication in social systems. Since dynamic social systems are fluid, changing,
emergent, developing, and yield created information in a meaning-making process, it fol-
lows that dynamic systems research best serves scientific discovery by substantiating these
same processes in the method. The dynamic systems methods presented here place the sci-
entist in the system, not knowing the answer, but working through a dynamic process of en-
gagement with the system, toward an emergent understanding of the patterns of communi-
cation and their changes over time with respect to the limitations of the observer’s method
and point of view.
Introduction
Dynamic systems theory addresses the problem of describing the ways in which
complex systems change over time. The focus of this paper is to highlight the unique
conceptual and research issues that arise when change in social communication sys-
tems is the topic of investigation. Specifically, in addition to quantitative indices of
change in frequencies, durations, and sequential patterning of communicative behavior,
research on communication can also encompass the meaning in the system. Meaning,
similar to any other pattern formation process in a dynamic system, can be thought of
as emerging and stabilizing dynamically through a process of self-organization. This
paper presents a research model that includes both developmental changes in quantity
and in meaning. These terms are defined and the methods are explained and illustrated
in a lengthy research example.
The study of change is paradoxical. The phenomenon that one wishes to observe
in one moment is no longer the same in the next moment. Yet, as human observers, we
are capable of perceiving and describing when behavior at two or more moments in
time appears to be the “same” or “different” (Popper, 1968). This is particularly rele-
vant to the problem of studying communication because meaning can be defined as
7
8 ALAN FOGEL
the perception of a “difference” between two or more communicative actions. But the
meaning of the perceived difference can only become manifest in the changing actions
or interpretations of participants in a communication process. Meaning-making is thus
part of the way in which human observers interpret some complex series of changes
as “having” a pattern, structure, or order. Any time an observer declares the presence
of a pattern, in other words, the observer becomes a part of the dynamic system being
observed. The stars in a galaxy do not in fact have, own, or possess a pattern. The pat-
tern (the galaxy) emerges in the relationship of the stars to the observer.
The study of complex dynamic systems takes as a premise that individual compo-
nents and constituents are best understood as part of a collective in which each affects
the others to create pattern and order at the level of the collective, an order which may
not be obvious at the level of the behavior of each of the constituents. This paper takes
the perspective that the study of dynamic systems involves one additional constituent
to any collective that is being observed: the observer’s point of view. The observer, in
other words, is part of the description or model of the system. Although complex sys-
tems exist in the absence of the observer, the patterns and processes that are described,
counted, and analyzed emerge from the relationship between the observer and the sys-
tem. This point refers to the role of scientists on systems in which they are not partic-
ipants. Should they be participants, their behavior and presence becoming part of the
system, in addition to their point of view contributing to how that system comes to be
understood by others?
The pattern, furthermore, emerges over some finite period of time. One looks at
the world and patterns seem to appear instantaneously. There is, however, at least
some period of microseconds required for the brain and sense organs to organize the
perceptual flow into a flower, tree, or galaxy. Even that relatively rapid emergent
process, however, is founded upon an earlier, and considerably longer, period of en-
gagement in that person’s life, a period in which patterns were not apparent and
needed days, weeks, or months to be discovered through some process of engagement
with the world. The pattern coalesces and stabilizes into a consistent attractor in the
brain-behavior-sensory system, making the recognition of the pattern on future occa-
sions more rapid and efficient (Lewis, 1995; 2005; Thelen & Smith, 1994).
This longer process of meaning-making could, of course, be applied to an infant
or child who must discover through perception and action, or “re-create,” the mean-
ings of words and gestures via a process of co-regulation with adults (Fogel, 1993;
King, 2004). In this paper, however, we apply the same notion to the scientist. Faced
with a complex system whose patterns do not easily appear to the observer, patterns
may—through a process of prolonged engagement, discovery, and meaning-making—
finally emerge.
It is not the intention here to review the growing literature on dynamic systems re-
search and theory. Where needed, the principles of dynamic systems theory are briefly
mentioned. The central theme of dynamic systems theory is to understand how the pat-
terning of the collective is related to the co-regulation between the constituents. In the
view of dynamic systems theory, the constituents of a system act together to constrain
the multiple actions of other constituents so that the complex system organizes and re-
organizes over time into a series of semi-stable patterns of behavior called attractors
Dynamic Systems Research on Interindividual Communication 9
(Kelso, 1995; Kugler, Kelso, & Turvey, 1982; Prigogine & Stengers, 1984). Con-
stituents, in other words, change each other in the process of convergence toward an
attractor. Two people in a long-term partnership change each other in the process of
forming a “couple” with recognizable patterns and habits.
Each time an attractor is re-constituted, the actions within the attractor, the mi-
crolevel activity of the system, are somewhat different from the previous occurrence
of that same attractor. The concept of dynamic stability replaces the concept of struc-
ture, habit, and association in traditional theories of behavior regularities (Capra,
1996; Fogel, 1993; Thelen & Smith, 1994). The attractor occurs at an organizational,
collective, or macrolevel of activity, in which the observer’s perception of “sameness”
becomes possible.
In the behavioral sciences, complex systems occur for intraindividual, interindi-
vidual, ecological, and sociocultural relationships. The intraindividual system in-
volves relationships between the various systems of the body and mind, such as be-
tween genes and their cellular environment, between brain and behavior, between
muscles that act together to perform an action, or between emotion and intellect. The
interindividual system involves social relationships such as between parent-child,
close companions, teacher-student, supervisor-employee, therapist-client, romantic
partners, and business partners. The ecological system includes relationships between
humans and their physical and biological environment such as our relationships with
the plants, animals, and the earth. The sociocultural system contains all the relation-
ships within and between groups of people with intersecting histories; it takes in rela-
tions of international peace or conflict, systems of kinship and religion, of politics and
economics, institutions of education or medical care, systems of government and law.
changed. Buber (1958) called these types of relationships “I-Thou” as opposed to the
totalizing stance of “I-It” relationships.
Scientists who take as the starting point the slipperiness and ineffability of the very
dynamics that they wish to study may aspire to shed light on the underlying dynam-
ics of behavior. No previous reification of behavior dynamics has succeeded in help-
ing us understand why some people contract deadly diseases, why war and violence
continue to flare in an enlightened global society, or why poverty and hunger are glob-
ally pervasive. Perhaps the answers lie in a dynamic understanding of how these prob-
lems develop over time. Perhaps there are no concrete answers, but rather a process of
learning how to understand and work with our unimaginably complex universe.
facial movement requiring little energy can induce large expenditures of movement en-
ergy in the social partner, as when a smile elicits a partner’s heart rate change and ini-
tiates movements of approach. Intracellular communication via the different sequences
of bases in DNA and neural communication via different neurotransmitters are other
examples of informational dynamic systems (Capra, 1996; Oyama, 1985; Pattee, 1987).
This information approach has an emphasis on the mutuality between constituents
which change as they enter into relational processes, altering their identities in order
to establish the ground for a relationship. A facial expression, such as a smile, does not
contain discrete information about the smiler. Rather, the meaning of the smile de-
pends upon the relationship between the smiler and the partner. People do not typi-
cally smile unless the partner is perceived as receptive to opening that line of emo-
tional communication.
In digital and electronic systems, information is usually thought of as discrete bits
having a concrete value (either “on” or “off” in a binary system typical of most com-
puters). A dynamic system, however, requires a completely different conceptualization
of information that is not fixed in advance and not “transmitted.” Rather, information
is created in the process of communication and is always dynamically related to the
current state of the entire developing system (Fogel, 1993; Oyama, 1985). In other
words, meaning making is the outcome of a finite process of engagement.
In another example, long-term social partners develop between them informational
attractors involving unique patterns of speech and expression not shared outside the
relationship. Words and gestures of endearment for a romantic couple (sweetie, lover,
honey, etc.) mean (are informed by) the entire history of their communication, re-
creating particular feelings and perhaps further states of intimacy. Yet, words and ges-
tures are not fixed in form and usage. “Honey” can be spoken with love, anger, or im-
patience depending dynamically on the situation. “Honey,” while meaningful to the
partners, does not always mean the same thing because the information is created in
the moment of dynamically unfolding feelings and actions.
variations often occur spontaneously, such that development emerges from the activity
of the system itself (Fogel et al., 2006a; Thelen & Smith, 1994; van Geert, 1998). Dy-
namic systems, in other words, are historical. The available set of attractors serves as re-
sources for the system to create opportunities for developmental change. The same idea
is contained in Piaget’s (1954) thinking: that some chance discovery may eventually
change the existing system of schemes via assimilation and accommodation.
The problem of the emergence of new forms is at the very core of developmental
inquiry. How does something new emerge from something that has been there in rel-
atively stable form? Dynamic systems theory recognizes the emergence of innovation
or novelty as a fundamental feature of complex systems. Non-biological systems, such
as chemical reactions and the physical universe, develop over time because novel vari-
ability provokes the system into new stable attractors that are neither planned nor pre-
programmed (Laszlo, 2001; Prigogine & Stengers, 1984; Weimer, 1987). A growing
number of thinkers have embraced the idea that spontaneous emergence is at the heart
of behavioral and psychological change. In the behavioral sciences, this concept has
also been called discovery, creativity, construction of novelty, and transformation
(Carvalho & Pedrosa, 1998; Eckerman, 1993; Fogel, 1993; Gottlieb, 1992; 2003;
Lewis, 1995; Lock, 1980, 2000; Lyra, 1998; Mahoney & Moes, 1997; Nelson, 1997;
Overton, 2002; Schore, 2003; Stern, 1998; Thelen & Smith, 1994; Tronick, 1998;
Valsiner, 1997; 2001).
The indeterminacy in dynamic systems can produce historically unique trajectories
that partly account for the formation of individual differences (Fogel, 1990; Fogel &
Branco, 1997; Fogel, Lyra, & Valsiner, 1997; van Geert, 1997; Kellert, 1993; Thelen,
1990; Valsiner, 1997). Informational approaches to dynamic systems perspectives can
help us understand why historical changes in people, groups, or societies can never ex-
actly repeat, why every social system is unique, and why these differences are contin-
gent on the dynamics of the communication process and not always amenable to pre-
diction (Fogel, Lyra, & Valsiner, 1997; Gould, 1977).
t = observation interval
T = developmental interval
t < < T
FIGURE 1.
18 ALAN FOGEL
ducted before and after the change takes place. The change may be a sponta-
neous developmental change or it may be a planned intervention.
• There is an elevated density of observations within the transition period. That
is, observations are conducted at time intervals that are considerably shorter
than the time intervals required for the developmental change to occur. For in-
stance, if a developmental change takes place over several months, then obser-
vations should be conducted weekly or even more frequently.
• Observed behaviors are intensively analyzed, both qualitatively and quantita-
tively, with the goal of identifying the historical processes that give rise to the
developmental change.
The unit of analysis is one of the types of systems described earlier: intraindivid-
ual, interindividual, ecological, and sociocultural. In the interindividual system, for
example, as an individual develops, its relation to the external world changes, such
that its effective environment—the actual physical, biological, and social factors with
which it interacts—also changes. One of the challenges of systems research is to in-
terpret the concept of environment in such a way that it incorporates an appropriately
dynamic view of the changing relations between the developing individual and his or
her context. This requires observation across representative developmental contexts to
identify the range of behavioral capacities and developmental trends characteristic of
the organism-environment system.
Microgenetic research has the advantage of being able to trace the historical devel-
opment of change over time within the same system. The historical approach has been
applied using microgenetic research designs (Bruner, 1983; Fogel, 1990; Fogel et al.,
2006a; Granott & Parziale, 2002; Greenspan, 1997; King, 2004; Lavelli et al., 2005;
Overton, 2002; Rosenwald & Ochberg, 1992; Shanker & King, 2002; Siegler & Crow-
ley, 1991; Thelen & Smith, 1994; van Geert, 1998). These studies involve both quan-
titative tracking of developmental trajectories and qualitative analysis of life history
narratives that reveal developmental shifts in shared information relative to new be-
havior coordinations in interindividual systems.
Recent advances have given dynamic systems scientists new tools for the study of
change processes. There now exists a new class of statistical models called hierarchi-
cal linear models or multilevel models (Bryk & Raudenbush, 1992; Butt, Choi, &
Jaeger, 2005; Prosser, Rasbash, & Goldstein, 1991) that allow researchers to examine
developmental trajectories in microgenetic designs, made by tracking a key measure
over frequent observations, for the group as a whole and for each individual. There
have also been recent improvements in qualitative research methods, giving new cred-
ibility and rigor to the use of narrative descriptions of observed behavior and life his-
tory narratives (Denzin & Lincoln, 1994; Polkinghorne, 1995). These new quantita-
tive and qualitative methods fit perfectly with the focus of dynamic systems on change
over time in the qualitative macroscopic attractors.
In addition to observations of the natural evolution of systems, systems research
often includes systematic experimental intervention or manipulation to uncover and
identify the developmental resources necessary and sufficient to foster developmental
change. In the intraindividual and interindividual systems, these resources include
genes, cell and tissue interactions, sensory experience, diet and exercise, and social re-
lations with conspecifics, to name but a few.
Dynamic Systems Research on Interindividual Communication 19
Dynamic systems experimental interventions or manipulations attempt to discover
the differences that make an impact by following developing systems as they develop
and add or subtract features of normally occurring experience or activity to identify
those developmental resources and their relationships that are necessary and sufficient
to foster change. These differences are hypothesized to be innovations that have the
potential to alter the system. The key idea is that the experimental alteration must
never be so drastic as to destroy the possibility for the system to transform over time.
The following are examples of dynamic systems experimental procedures (Gottlieb &
Lickliter, 2004; Lickliter & Honeycutt, 2003).
1. Experiential attenuation is when features of normally occurring experience are
removed from the developmental context, allowing researchers to better identify
how change is influenced by specific developmental resources in real time.
2. Experiential enhancement is when additional experience is added to the in-
dividual’s developmental context. This can be done by experiential substitu-
tion, in which normally occurring experience is replaced with a different form
of experience, or experiential displacement, in which the temporal relations
between features of experience are shifted or rearranged to allow deeper in-
sight into the history or process of specific reorganizations.
These types of manipulations and the evaluation of their consequences on devel-
opmental change are often used in parallel with one another to explore the complex-
ity and contingency of developmental processes. Combining microgenetic observa-
tion, which documents the process of change, with experimental manipulation, which
identifies the developmental resources contributing to change, provides a powerful
method for identifying the conditions under which change is most likely to occur.
In summary, dynamic systems research:
1. seeks primarily to probe the systemic and simultaneous linkages in the network
of relationships that sustain particular patterns of development over time;
2. aims to uncover the possible pathways that lead to changes in certain undesir-
able patterns; and
3. attempts to discover the processes required to sustain and foster the develop-
ment and maintenance of a healthy developmental trajectory, or a more desir-
able network of relationships needed for effective decision-making and posi-
tive social change.
In intervention research, for example, systems don’t get “fixed” or “cured” with a
simple formula. Rather, the dysfunctional system must be allowed to transform slowly
over time, systemically, into a more functional system. In dynamic systems science,
we seek to understand the laws of transformation.
Research Example
It is difficult to present a complete dynamic systems research example in the short
space of this paper. Many more detailed examples of qualitative dynamic systems
22 ALAN FOGEL
research using these principles can be found in Fogel et al. (2006a), King (2004), and
Fogel, King, & Shanker (2006). In addition, a description of applied dynamic systems
research methods is given in Fogel, Greenspan, King, Lickliter, Reygadas, Shanker &
Toren (2006).
Here, an excerpt is presented from Fogel et al. (2006a) that illustrates the descrip-
tion of a developmental (Level 3) change in one mother-infant dyad during the period
between 2 and 6 months. The attractors of interindividual relationships are regularly re-
curring patterns of communication called frames. Frames are segments of co-action
that have a coherent theme, that take place in a specific location, and that involve par-
ticular forms of mutual co-orientation between participants. Because frames recur re-
peatedly over weeks and months, they have the features of an attractor in a dynamic
system since they are reconstituted dynamically and dyadically on each reappearance.
Frames are semi-stable, lasting for only a finite period in an interindividual relation-
ship. They emerge at one point in time and dissolve or disappear at another point in
time. In a romantic partnership, for example, engagement or betrothal is a frame that
has a limited time of life between courtship and marriage.
The communication between the 13 mother-infant dyads in this study was video-
taped weekly during the 4-month observation period, meeting the conditions for a mi-
crogenetic research design (Figure 1). These videos were coded into four mutually ex-
clusive and exhaustive relationship frames. The social frame was coded when the
topic of communication was face-to-face play without objects. The guided object
frame was coded when the mother took an active role in demonstrating and scaffold-
ing the infant’s use of objects. The non-guided object frame was coded when the in-
fant played with objects without the mother’s direct assistance but with her ongoing
attention and verbal commentary. The social-object mixed frame was coded when el-
ements both of face-to-face play and guided-object play appeared at the same time, as
when a mother used a toy to touch the infant’s face or body while vocalizing in an ex-
pressive manner typical of the social frame.
The durations of each of the frames, measured as a percentage of time in the ob-
servation session (sessions lasted 10 minutes) is shown graphically in Figure 2 for one
dyad, Betsy and her mother. Notice that the durations of the social and the guided-
object frames decline over this period, while the not-guided-object frame and the
social-object mixed frame increase in duration.
In this example, the focus is on the sessions in which developmental change is
most rapidly occurring, sessions 7 and 8, in which Betsy is 17 and 19 weeks old. Dur-
ing session 6, Betsy for the first time reaches for an object while looking at it. In ses-
sion 7, the social frame declines dramatically. Betsy continues to look at her mother
and smile during the other frames, thereby maintaining a connection with her mother,
and thus blending the social frame into the other frames. This is seen especially in the
rapid increase in duration of the social-object mixed frame. Sessions 7 and 8 are the
first time that the not-guided object frame emerges as an entirely new frame, separate
from the other object-related frames, in which Betsy explores objects without the
mother’s assistance (as in the guided object and social-object mixed frame).
With the increasing growth of the not-guided-object frame, the guided-object
frame, while actually declining quantitatively over time, continues to develop qualita-
Dynamic Systems Research on Interindividual Communication 23
DYAD: 13
100
Social
90
Guided Object
80
Not-Guided Object
70 Social-Object Mixed
% of Session
60
50
40
30
20
10
0
1 2 3 4 5 6 7 8 9 * * *
Session
FIGURE 2.
tively. The mother, for example, gives Betsy certain objects and helps her hold them
when needed.
The not-guided-object frame and the guided-object frame now occur in quick succession.
Object manipulation follows a sequence composed of: Betsy actively mouthing an object
(i.e., the not-guided-object frame), the mother introducing a new object to Betsy followed
by Betsy reaching for and grasping the new object (i.e., the guided-object frame), and then
Betsy manipulating the second object, at times actively mouthing it (i.e., the not-guided-
object frame). This sequential patterning between the guided-object and the not-guided-
object frames appears to constitute a form of historical recapitulation in which an already
existing historical frame (i.e., the guided-object frame) is maintained and makes transitions
with a newly emergent frame (i.e., not-guided-object frame).
Now that Betsy is becoming more skilled at manipulating objects on her own, a new or-
dinary variability characterizing the social-object mixed frame also emerges during visits 7
and 8. The mother now uses the object Betsy is holding, making it kiss Betsy’s face without
taking the object from her. It is as if Betsy is playing the object-touch games herself. Both
Betsy and her mother are also becoming more serious, smiling and laughing relatively little
and producing fewer vocalizations. The mother, for instance, uses far fewer sound effects
with objects during visits 7 and 8. The impression the observer gets is that the social-object
mixed frame is gradually becoming transformed as the not-guided-object frame emerges as
a new and distinct frame. In fact, certain characteristics of the not-guided-object frame (such
as helping Betsy play the object-touch games herself) appear to permeate the social-object
mixed frame. (Fogel et al., 2006a)
These two sessions not only show a quantitative change in the frame durations, but
there was also a qualitative change in the pattern of organization, both at the microlevel
within the frames and the macrolevel of sequencing between the frames for Betsy and
her mother. This complex system of linked changes constitutes a developmental (Level
3) change. The developmental change is not merely in the fact that the not-guided-
24 ALAN FOGEL
object frame emerges for the first time, but rather because the whole system of frames
seems to shape-shift in order to give birth to the new frame. All these changes are oc-
curring simultaneously, as a dynamic process rather than a simple sequence.
The not-guided-object frame begins to pervade these sessions with the “support” of the
guided-object frame and the social-object mixed frame. Compared to previous sessions, all
of the observed frames (i.e., not-guided-object frame, guided-object frame, and social-
object mixed frame) undergo coordinated changes as reflected by the emergence of a new
ordinary variability for each of these frames. Specifically, as Betsy becomes more object-
focused and fascinated with the new activity of examining the objects around her, the
mother adjusts her object-oriented behaviors and begins providing support to her infant’s
object exploration by handing them to Betsy.
The not-guided-object frame begins to become elaborated into a fully developed frame
as Betsy spends increasing amounts of time manipulating objects. This constitutes a newly
emergent frame that arises out of the innovations (Level 2 change: the mother places objects
in Betsy’s hands) within the guided-object frame and social-object mixed frame during ses-
sions 4, 5, and 6. At the same time, the guided-object frame expands its forms as illustrated
by the increasing variability in the way the mother presents objects to Betsy. The social-
object mixed frame also changes from its earlier quality of enjoyable social play to becom-
ing more focused on Betsy’s more serious examination of objects.
Furthermore, the dyad’s new ordinary variability (Level 1 change) during sessions 7 and
8 includes a patterned integration of the guided-object frame and the not-guided-object frame.
In this case, it is as if frames (i.e., guided-object frame and not-guided object frame) are blend-
ing together at the same time that a historical dynamic is recapitulated by the dyad.
All of these processes—the simultaneous re-organization of each of the frames in relation
to each other and the emergence of a new frame in the context of the blending and recapitula-
tion of frames—constitute what we consider to be the conditions of a developmental change
(Level 3 change). Innovations (Level 2 change), as seeds for developmental change, alter the
ordinary variability within frames on later occasions. This alteration, however, is of the same
kind as the innovation when the infant becomes more active across multiple modalities. In the
case of this developmental change, however, the entire pattern of communication changes
across the whole system: all the frames and transitions are involved. For reasons we do not yet
understand, the build-up and elaboration of innovations seems to reach a critical point at which
time the “old” or historical system can no longer contain the innovations within ordinary vari-
ability. At this time, the system spontaneously shifts to a new system-wide organization that
includes new frames, creative blending of old frames, and new actions within frames. It is im-
portant to note that we did not observe any single innovation or event that precipitated the de-
velopmental transition. (Fogel et al., 2006a)
Although the more detailed account cannot be given here, this excerpt shows the focus
on history and meaning, the role of the observer, and the complexity of the co-actions
across all three levels of change in the system. It also shows that a qualitative analy-
sis provides something that cannot be gleaned from the quantitative description alone.
The two methods, quantitative and qualitative, support and complement each other as
a description of the developmental change process.
The tools are now available to address these types of research questions, but these
methods are slower and cost more than conventional research. This is because it is nec-
essary to wait for the change to unfold, and many observations must be made in order
to track the change process. The gain in understanding, however, is likely to be high.
Qualitative dynamic systems research is ideal for translational applications. Mod-
els that are expressed in terms of statistical interactions between quantitative variables
are probabilistic and often far removed from the everyday process of meaning making
as a social system. New models and interventions that rely on an understanding of the
informational dynamics of the change process could be immediately applied to the
work of practitioners and participants because these models are expressed in terms of
the meanings that are already present in the system.
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Early Family Trauma and the Ontogeny of
Glucocorticoid Stress Response in the Human
Child: Grandmother as a Secure Base
Mark V. Flinn
Department of Anthropology and
Department of Psychological Sciences
University of Missouri
FlinnM@Missouri.edu
David V. Leone
Department of Anthropology
University of North Carolina
Abstract: Loss of a parent by death or divorce is among the most traumatic experiences
faced by a human child. Exposure to early family trauma (EFT) can have long-term effects
on the limbic hypothalamic-anterior pituitary-adrenal cortex (HPA) axis and other compo-
nents of neuroendocrine stress response. Because the HPA system has important immuno-
modulatory functions, children that have endured difficult family social conditions during
development may be at higher risk for immune dysfunction and other health problems.
Here we investigate the mediating effects of grandparental relationships, mostly maternal
grandmothers, on the ontogeny of HPA stress response among EFT children.
31
32 MARK V. FLINN AND DAVID V. LEONE
1. This three year-old child referred to her grandmother as “Mama,” and her mother by her given name.
2. All place names and research participant names used here are pseudonyms to protect privacy rights.
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 33
view the potential functions of physiological stress response to stimuli in the social en-
vironment. We then investigate the effects of grandparents on the ontogeny of stress
response among children that have endured the loss of a parent by death or separation.
2005; Meaney, 2001; Pitman, 1989; Rodriguez Manzanares, Isoari, Carrer, & Molina,
2005). For example, in the relatively straightforward prey-predator situation of a
gazelle smelling a lion, a “freeze” response, focused sensory acuities, and neurologi-
cal circuits for escape behaviors may be enabled. The human child may face more
cognitively challenging problems that use more information processing capacity, such
as complex social interactions (Roth & Dicke, 2005). For example, when dealing with
the challenge of making friends on the first day of school, a child needs to allocate her
cognitive efforts to the tasks at hand: prepare for immediate contingencies by recall-
ing salient information, enhancing relevant sensory input, and pre-activating circuits
for appropriate actions. Stress hormones may enable not only the acute responses to
such challenges, but facilitate their modification during development as well. Parents
and grandparents may play an important role in this dynamic interplay between stress
response to social challenges and the ontogeny of a child’s coping mechanisms by pro-
viding both security and information.
Hypotheses are evaluated with analyses of data from an 18-year study of child
stress in a rural community on the island of Dominica. The longitudinal depth, large
sample size (30,122 salivary cortisol measures from 282 children and their care-
givers), and naturalistic paradigm provide a unique research design for investigating
relations between social environment and ontogeny of stress response. Empirical
analysis is complicated by the pleiotropic nature of the key stress hormone cortisol.
Moreover, the Dominica study does not have neurological data, hence direct or strong
demonstrations of causal links among stress response, neural plasticity, family envi-
ronment, grandparental care, and ontogeny of social competencies are not possible.
Our initial objective here is to review a plausible model that links stress response
to the neural plasticity that enables adaptation to the dynamic human social environ-
ment. We then assess the effects of early family trauma on the ontogeny of stress re-
sponse, and the potentially ameliorative effects of grandparental care. Understanding
these relations may have significant consequences for child development and public
health because it could provide new insights into associations among stress response,
social disparities, and perinatal programming, among other outcomes (Barker, 1998;
Dressler, Oths, & Gravely, 2005; Heim & Nemeroff, 2001; Maccari, Darnaudery,
Morley-Fletcher, Zuena, Cinque, & Van Reeth, 2003; Marmot, 2004).
10:10 July 13 10
3 17:35 July 17
Ordered down
Runny nose,
from tree
cough, oral
2 temp. = 101.2°F
s-IgA mg/dl
1
Cortisol z-score
–1
–2 0
13 14 15 16 17
July
four years, since his father had left when James was three years old and his stepfather
had slowly moved in. James had always been close to his grandmother—whom he
called “Mama”—as well as his mother—whom he called by her given name Lily.
James’ cortisol levels were often elevated by family conflicts, but the solace he usu-
ally found at his grandmother’s often resulted in a return to normal levels.
These anecdotal case examples contribute to a common pattern. Children in this
rural Dominican community are more than twice as likely to become ill during the
week following a stressful event than during a week when they had not recently expe-
rienced any significant stressors (Flinn & England, 2003). Chronic elevation of corti-
sol levels may have negative consequences for health (Cohen, Doyle, Turner, Alper &
Skoner, 2003; Maier, Watkins, & Fleschner, 1994; Marmot & Wilkinson, 1999;
Mason, Buescher, Belfer, Artenstein, & Mougey, 1979). Morbidity and mortality rates
for children in the stressful environments of orphanages and hospitals, if lacking the
evolutionarily-normal intimacy and social contact of the family, can be a significant
public health concern worldwide. It is not lack of food or hygienic care, nor just the
occurrence of traumatic events that affect child health, but the lack of social support,
including parental warmth and other factors that influence emotional states (Belsky,
1997; Davidson, Jackson, & Kalin, 2001; Field, Diego, Hernandez-Reif, Schanberg,
& Kuhn, 2003). Why should this be so? Why do social interactions, and a child’s per-
ceptions of them, affect stress physiology and morbidity? And, more generally, why is
the social environment of such paramount importance in a child’s world? From the
Tinbergen perspective, these “why?” questions ultimately involve understanding the
evolutionary design of the ontogeny of the mind and brain of the human child (e.g.,
Belsky, 1997; Bjorklund & Pellegrini, 2002; Gilbert, 2005).
In Danny and James’ village, located on the east coast of the island of Dominica
where I have lived and studied part-time over the past eighteen years, most of a child’s
mental efforts seem focused on negotiating social relationships with parents, siblings,
grandparents, cousins and other kin, friends, teachers, bus drivers, neighbors, shop own-
ers, and so forth. Foraging for mangoes and guavas, hunting birds, or even fishing in the
sea from rock cliffs, are relatively simple cognitive enterprises, complicated by conflicts
with property owners, and decisions about which companions to garner and share calo-
ries with. The mind of the child seems more concerned with solving social puzzles than
with utilitarian concerns of collecting food. Other populations may have more difficult
subsistence practices that require more extensive learning (e.g., Bock, 2005), but the so-
cial chess game nonetheless appears ubiquitous and cognitively demanding in all cul-
tures (Blurton-Jones & Marlowe, 2002; Hewlett & Lamb, 2005), as it likely was during
human evolutionary history (Adolphs, 2003; Alexander, 1979, 1989; Baumeister, 2005;
Bowlby, 1969, 1973; Flinn, Geary, & Ward, 2005; Hinde, 1974).
Complex sociality appears to have been an important selective pressure shaping
the uniquely human combination of physically altricial but mentally and linguistically
precocial infancy, extended childhood, and extended adolescence, enabled by exten-
sive bi-parental and kin care (Alexander, 2005; Geary & Flinn, 2002; Flinn & Ward,
2005). Physiological stress response may help guide both the acute and long-term neu-
rological plasticity (Huether, Doering, Ruger, & Schussler, 1999) necessary for adapt-
ing to the dynamic aspects of human sociality (Flinn, 2006b). Grandparents may pro-
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 37
vide important advice and enhance a secure base for the stressful tasks involved in the
development of social competencies.
Grandparental Relationships
Caregiving by individuals other than parents provides important benefits for in-
fants and juveniles in a variety of taxa. “Helpers” in birds, rodents, social carnivores,
38 MARK V. FLINN AND DAVID V. LEONE
elephants, and non-human primates enhance growth and survival (e.g., Alexander,
Noonan, & Crespi, 1991; Brown, 1987; Clutton-Brock, 2002; Lee, 1987; Mitani &
Watts, 1997). Kin selection and reciprocity appear to provide the evolutionary func-
tions for non-parental care providers. Among primates, intensive allomaternal care-
giving (e.g., feeding, carrying) is common in the callitrichids (e.g., Goldizen, 1987)
and the colobines. Allomaternal care among the cercopithecines (e.g., Fairbanks,
1990; Maestripieri, 1994) and hominoids (e.g., Goodall, 1986; Nishida, 1990) is usu-
ally limited to protection from conspecifics and predators. Practice care is generally
common among nulliparous females in social species (e.g., Hrdy, 1999). The preva-
lence of extensive alloparental care among humans (e.g., Flinn, 1989; Lahdenpera,
Lummaa, Helle, Tremblay, & Russell, 2004; McKenna, 1982; Sear, Mace, & McGre-
gor, 2000, 2003; Silk, 1990; Strassmann & Clarke, 1998; Tronick, Morelli, & Winn,
1987; Tronick, Morelli, & Ivey, 1992), particularly the importance of grandparents for
direct care (Alexander, 1979; Hawkes, 2003), represents a strong divergence from our
closest primate relatives.
The conditions responsible for the evolution of extensive alloparental care in hu-
mans are likely to include the importance of localized kin groups, altricial infants, pro-
longed childhood, extended generational overlap, and the cultural transmission of in-
formation (Alexander, 1989; Coe, 2003; Flinn & Ward, 2005; Geary & Flinn, 2001;
Hrdy, 2005). Grandparents appear to be the most significant of potential alloparental
caregivers (Hrdy, 2005).
The informational arms race that characterizes human social competition involves
substantial novelty (Flinn, 2004, 2006a; Flinn & Alexander, 2006; Flinn & Coe, 2006)
and hence requires unusual phenotypic plasticity. Although knowledge of the basic
neuroanatomical structures involved with human social aptitudes has increased dra-
matically (e.g., Allman, 1999; Damasio, 2003; Gallese, 2005; Moll, Zahn, de Oliveira-
Souza, Krueger, & Grafman, 2005), the mechanisms that guide their ontogeny remain
uncertain. Neuroendocrine stress response to stimuli in the social environment may
provide important clues.
wide range of health effects of stress suggests that a number of immune mechanisms
are involved. Cortisol influences many functions of lymphocytes, macrophages, and
leukocytes, and as with energy use, may direct their movement to specific locations
and even modulate apoptosis (Costas et al., 1996). Cortisol also inhibits the produc-
tion of some cytokines (e.g., interleukin-1) and mediates several components of the in-
flammatory response. In concert with the sympathetic system, which generally down-
modulates lymphocyte and monocyte functions, HPA stress response affects all of the
major components of the immune system. However, the effects of neuroendocrine
stress response are not all inhibitory, and involve temporary up-regulation and/or lo-
calized enhancement of some immune functions (Dhabbar & McEwen, 2001; Jef-
feries, 1991; Coe & Lubach, 2005).
Stress response involves an optimal allocation problem (Sapolsky, 1990a, 1994). En-
ergy resources are diverted to muscular and immediate immune functions and other
short-term (stress emergency) functions, at cost to long-term functions of growth, devel-
opment, and building immunity. Under normal conditions of temporary stress, there
would be little effect on health. Indeed, there may be brief enhancement and directed traf-
ficking of immune (Dhabbar & McEwen, 2001) and cognitive function. Persistent stress
and associated hyper- or hypo-cortisolemia, however, is posited to result in pathological
immunosuppression, depletion of energy reserves, and damage to or inhibition of neuro-
genesis in parts of the hippocampus (e.g., Gould & Tanapat, 1999; Santarelli, Saxe,
Gross, Surget, Battaglia, Dulawa, Weistaub, Lee, Duman, Arancio, Belzung, & Hen,
2003; Sheline, Gado, & Kraemer, 2003). This perspective highlights the problems with
a stress response system that evolved to cope with short-term emergencies. The chronic
stress produced by modern human—or other primates with complex relationships—
social environments may present novel challenges that the system is not designed to han-
dle, hence potentially resulting in maladaptive pathology (Sapolsky, 1994, 2003).
This strict version of an environmental novelty hypothesis, however, is difficult to
reconcile with the long evolutionary histories of complex sociality in primates, and es-
pecially humans, accompanied by dramatic changes in the brain. Why, given all the
extensive modifications of the human brain over the past several million years, would
selection not have weeded out this apparent big mistake? Modern human environ-
ments have many novelties that elicit stress response, but social challenges in general
seem to have a much more ancient evolutionary depth, and may be a key selective
pressure for the large human brain. One possibility is that the demands of preparing
for potential dangers are an unavoidable costly insurance, akin to expensive febrile re-
sponse to pathogens that are usually benign—the “smoke-detector” principle (Nesse
& Young, 2000). The idea is that although physiological stress response to social chal-
lenges is costly, and most often wasteful, it may have helped our ancestors cope with
rare and unpredictable serious conflicts often enough to be maintained by selection.
The benefit/cost ratio could be improved by fine-tuning stress mechanisms in response
to environmental conditions during ontogeny.
A complementary approach suggests that neuroendocrine stress response may
guide adaptive neural reorganization, such as enhancing predator detection and avoid-
ance mechanisms (Buwalda, Kole, Veenema, Huininga, De Boer, Korte, & Koolhas,
2005; Dal Zatto, Marti, & Armario, 2003; LeDoux, 2000; Rodriguez Manzanares
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 43
et al., 2005; Meaney, 2001; Wiedenmayer, 2004). Exposure to cats that elevates glu-
cocorticoid levels can have long-term effects on the central amygdala (right side) in
mice, resulting in increased fear sensitization (Ademec et al., 2005; see also Knight,
Nguyen, & Bandettini, 2005). The potential evolutionary advantages of this neural
phenotypic plasticity are apparent (Rodriguez Manzanares et al., 2005). Prey benefit
from adjusting alertness to match the level of risk from predators in their environ-
ments. Post-Traumatic Stress Disorder (PTSD) appears analogous to these fear condi-
tioning models, and involves similar effects of noradrenergic (Pitman et al., 2002) and
glucocorticoid systems (Roozendaal, 2002; Roozendaal, Quirarte, & McGaugh, 2002)
on associative long-term potentiation of the amygdala. Social defeat also affects the
amygdala and hippocampus, but in different locations (Bartolomucci, Palanza, Sacer-
dote, Panerai, Sgoifo, Dantzar, Parmigiani, 2005; Buwalda, Felszhegy, Horvath,
Nyakas, de Boer, & Bohus, 2001; Koolhaas, de Boer, de Ruiter, Meerlo, & Sgoifo,
1997), suggesting that neural remodeling and LTP is targeted and domain-specific
(e.g., Pham, McEwen, Ledoux, & Nader, 2005; Rumpel, LeDoux, Zador, & Malinow,
2005). Glucocorticoids, perhaps in combination with peptide hormones and cate-
cholamines, appear to facilitate the targeting of domain-specific remodeling and long-
term potentiation (Huang & Herbert, 2006). The potentiating effects of cortisol on
emotional memories and other socially salient information may be of special sig-
nificance in humans (Fenker, Schott, Richardson-Klavehn, Heinze, & Düzel, 2005;
Jackson, Payne, Nadel, & Jacobs, 2006; Lupien et al., 2005; Pitman, 1989). The neu-
rological effects of stress response may underlie adaptation to both short-term contin-
gencies and guide long-term ontogenetic adjustments of behavioral strategies.
If physiological stress response promotes adaptive modification of neural circuits
in the limbic and higher associative centers that function to solve psychosocial prob-
lems (Huether et al., 1999), then the paradox of psychosocial stress would be partly
resolved. Temporary elevations of cortisol in response to social challenges could have
advantageous developmental effects involving synaptogenesis and neural reorganiza-
tion (Buchanan & Lovallo, 2001; Huether, 1996, 1998) if such changes are useful and
necessary for coping with the demands of an unpredictable and dynamic social envi-
ronment. Elevating stress hormones in response to social challenges makes evolution-
ary sense if it enhances specific acute mental functions and helps guide cortical re-
modeling of “developmental exuberance” (Flinn, 2006b; Innocenti & Price, 2005; Sur
& Rubenstein, 2005).
Chronic destabilization of neuronal networks in the hippocampus or cerebral cor-
tex, combined with enhanced fear circuits in the amygdala (e.g., Bauer, LeDoux, &
Nader, 2001; Phan, Fitzgerald, Nathan, & Tancer, 2006), however, could result in ap-
parently pathological conditions such as PTSD (Tupler & DeBellis, 2006; Yehuda,
2002) and some types of depression (Preussner, Baldwin, Dedovic, Renwick, Khalili
Mahani, Lord, Meaney, & Lupien, 2005). Even normal (but rather novel) everyday
stressors in modern societies, such as social discordance between what we desire and
what we have (Dressler & Bindon, 2000), might generate maladaptive HPA response.
Individual differences in perception, emotional control, rumination, reappraisal, self-
esteem, and social support networks seem likely co-factors (see also Ellis, Jackson, &
Boyce, 2006).
44 MARK V. FLINN AND DAVID V. LEONE
Testing these ideas about relations between physiological stress response, neural
remodeling, and adaptation to the social environment is not a simple or easy task (e.g.,
Pine, Fyer, Grun, Phelps, Szesko, & Koda, 2001). Cortisol can affect cognitive func-
tioning, and cognitive processing can affect cortisol response, all in an ongoing onto-
genetic dance. Teasing out the causes and effects in ontogenetic sequence requires
sequential data on physiological response profiles, environmental context, and
perception. Extensive research on hormonal stress response has been conducted in
clinical, experimental, school, and work settings (Dickerson & Kemeny, 2004; Gun-
nar, Tout, de Haan, Pierce, & Stansbury, 1997; Panter-Brick & Pollard, 1999; Stans-
bury & Gunnar, 1994; Weiner, 1992). We know relatively little, however, about stress
neuroendocrinology among children in normal everyday (“naturalistic”) environ-
ments, particularly in non-industrial societies (Panter-Brick, 1998). Investigation of
childhood stress and its effects on development has been hampered by the lack of non-
invasive techniques for measurement of stress hormones. Frequent collection of
plasma samples in non-clinical settings is not feasible. The development of saliva im-
munoassay techniques, however, presents new opportunities for research on stress re-
sponse to everyday life. Saliva is relatively easy to collect and store, especially under
adverse field conditions faced by anthropologists and psychologists working in natu-
ralistic research settings (Ellison, 1988). Longitudinal monitoring of a child’s daily ac-
tivities, stress hormones, and psychological conditions provides a powerful research
design for investigating naturally occurring stressors. Analyzing hormone levels from
saliva can be a useful tool for examining the child’s imperfect world and its devel-
opmental consequences, especially when accompanied by detailed ethnographic,
medical, and psychological information. Unfortunately, we do not yet have field tech-
niques for assessment of corresponding ontogenetic changes in the relevant neurolog-
ical mechanisms.
Our initial objective, back in 1989, was to assess what each child’s general stress
level was, as determined by a single measure of the level of cortisol in their saliva. The
idea was to see how this hormone was associated with a child’s family environment.
We assumed, rather naively, but in good academic company, that salivary cortisol
46 MARK V. FLINN AND DAVID V. LEONE
levels were a fairly stable “trait” character. What seemed like an unnecessarily cau-
tious decision at the time to collect and assay additional saliva samples from several
of the children resulted in a rather more complex study. We were quite surprised when
the results of the additional sample assays indicated that a child’s cortisol levels var-
ied substantially from one day to the next. Serendipity provided samples from two sib-
lings in good spirits one day, but sad and upset by a family quarrel the next, in con-
cert with field notes detailing the events. This temporal link between cortisol levels
and psychosocial states suggested a dramatic revision of research design. We also
were fortunate to have saliva samples from different times of day in this initial collec-
tion, and quickly recognized that very precise control of circadian patterns—in partic-
ular sleep schedules and wake-up times—was critical to accurate assessment of HPA
stress response (Flinn & England, 1992). More than 30,000 saliva samples later, it
seems we have more questions than answers.
In this study, sequential longitudinal monitoring is used to assess physiological
stress response to everyday events, including social challenges. Saliva is collected
from children by members of the research team at least twice a day, wherever the chil-
dren happen to be (usually at their household). This direct collection and observation
procedure avoids errors that can occur with at-home self- or parent-collection and re-
port protocols. The large sample size of cortisol measures for each child (>100 sam-
ples for most children) in a variety of naturalistic contexts provides a more extensive
and complex picture of HPA stress response than small sample designs.
Data analyses examine both long term (ten+ years) and short term (day-to-day,
hour-by-hour) associations among cortisol levels, family composition, socioeconomic
conditions, behavioral activities, events, temperament, growth, medical history, im-
mune measures, and illness. Physiological stress response is assessed by radioim-
munoassay (RIA) of cortisol levels in saliva. Analyses include mean values, varia-
tion, and day-to-day and hour-by-hour profiles of standardized (circadian control by
5-minute intervals from wake-up time) cortisol data (Flinn & England, 2003; Flinn &
Quinlan, in prep.). Family composition is assessed by age, sex, genealogical relation-
ship, and number of individuals in the caretaking household. Socioeconomic condi-
tions include household income, material possessions, land ownership, occupations,
and educational attainment. Caretaking is assessed by (a) frequencies and types of
behavioral interaction, (b) informant ratings of caretaking that children received, and
(c) informant interviews. Here we use a dichotomous (above median, below median)
composite measure of caretaking by grandparents (“GPC”). Immune response is as-
sessed by turbidimetric immunoassay of secretory-immunoglobulin A from saliva;
however, relatively few samples have been assayed (N = 212), and interpretation is
uncertain so inferences are preliminary. Health is assessed by (a) observed type, fre-
quency, and severity of medical problems (diarrhea, influenza, common cold, asthma,
abrasions, rashes, etc.), (b) informant (parents, teachers, neighbors) ratings, (c) med-
ical records, (d) growth (standard anthropometric measures, including height, weight,
and skinfolds) and fluctuating asymmetry patterns (Flinn, Leone, & Quinlan, 1999;
Leone, 2005) and (e) physical examination by a medical doctor. The primary measure
of health used is percentage of days ill, the proportion of days that a child was ob-
served (directly by researchers) with common benign temporary infectious disease
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 47
(89% were common-cold upper respiratory tract infections with nasal discharge,
cough, or myalgia—e.g., rhinovirus, adenovirus, parainfluenza, and influenza; 6%
were diarrheal; 5% were miscellaneous indeterminate—e.g., febrile without other
symptoms). Daily activities and emotional states are assessed from (a) caretaker and
child self-report questionnaires, and (b) systematic behavioral observation (focal fol-
low and instantaneous scan sampling). Multiple sources of information are cross-
checked to assess reliability (Bernard, Killwoth, Kronenfield, & Sailer, 1984).
In the following section we briefly review some of the results from this study that
may provide useful insights into the ontogeny of stress response to psychosocial chal-
lenges. We then turn to examining the effects that grandparents have in guiding this
aspect of child development.
3 family family
conflict returns
2
Cortisol (standardized)
–1
June 24 25 26 27 28 29 July 19 20 21 22
with family trauma. Some children had significantly elevated cortisol levels during
some episodes of family trauma but not during others. Cortisol response is not a sim-
ple or uniform phenomenon. Numerous factors, including preceding events, habitua-
tion, specific individual histories, context, and temperament, might affect how chil-
dren respond to particular situations.
Nonetheless, traumatic family events and social emotions such as guilt and shame
(Flinn, 2006c) were associated with elevated cortisol levels for all ages of children
more than any other factor that we examined. These results suggest that family inter-
actions were a critical psychosocial stressor in most children’s lives, although the sam-
ple collection during periods of relatively intense family interaction (early morning
and late afternoon) may have exaggerated this association.
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 49
Cortisol (standardized) 1
.5
–.5
Nuclear Nuclear Single Single Grand Grand Step Step Distant
father mother mother mother parents father father, relatives
abs > 50% + kin half-sibs
Household composition
Children residing in bi-parental, single mother with kin, and grandparental house-
holds have moderate cortisol levels (Figure 3), with a higher proportion of elevations
occurring in the context of positive affect situations such as competitive play, physi-
cal work, and excitement regarding novel situations.
Although elevated cortisol levels are associated with traumatic events such as fam-
ily conflict, long-term stress may result in diminished cortisol response. In some
cases, chronically stressed children had blunted response to physical activities that
normally evoked cortisol elevation. Comparison of cortisol levels during “nonstress-
ful” periods (no reported or observed crying, punishment, anxiety, residence change,
family conflict, or health problem during the 24-hour period before saliva collection)
indicates a striking reduction and, in many cases, reversal of the family environment-
stress association (Flinn & England, 2003). Chronically stressed children sometimes
had subnormal cortisol levels when they were not in stressful situations. For example,
cortisol levels immediately after school (walking home from school) and during non-
competitive play were lower among some chronically stressed children (cf. Long,
Ungpakorn, & Harrison, 1993). Some chronically stressed children appeared socially
“tough” or withdrawn and exhibited little or no arousal to the novelty of the first few
days of the saliva collection procedure. These subnormal profiles may be similar in
some respects to those of individuals with Post-Traumatic Stress Disorder (e.g.,
Yehuda, Engel, Brand, Seckl, Marcus, & Berkowitz, 2005).
Although elevated cortisol levels in children are usually associated with negative
affect, events that involve excitement and positive affect can also stimulate stress re-
sponse (Flinn, 2006c). For example, cortisol levels on the day before Christmas were
more than one standard deviation above normal, with some of the children from two-
parent households and those having the most positive expectations exhibiting the
50 MARK V. FLINN AND DAVID V. LEONE
highest cortisol (Flinn, 2006e). Cortisol response appears sensitive to social chal-
lenges with different affective states. Other studies further suggest that the cognitive
effects of cortisol may vary with affective states, such as perceived social support (Ah-
nert et al., 2004; Quas, Bauer, & Boyce, 2004).
There are some age and sex differences in cortisol profiles, but it is difficult to as-
sess the extent to which this is a consequence of neurological differences (e.g., Butler,
Pan, Epstein, Protopopescu, Tuescher, Goldstein, Cloitre, Yang, Phelps, Gorman, Le-
Doux, Stern & Silbersweig, 2005), physical maturation processes, or the different social
environments experienced, for example, during adolescence as compared with early
childhood (Flinn, Turner, Quinlan, Decker, & England, 1996; Flinn & Quinlan, in prepa-
ration). For instance, young adult women have a higher incidence of depression and as-
sociated abnormal cortisol profiles than children or young men in this community.
The emerging picture of HPA stress response in naturalistic context from the Do-
minica study is one of sensitivity to social challenges, consistent with clinical and ex-
perimental studies. The results further suggest that family environments are an espe-
cially important source and mediator of stressful social challenges for children. In the
next section, data on the longitudinal effects of early traumatic experiences are exam-
ined to assess the domain-specificity of changes in stress response.
Early experiences can have profound and permanent effects on stress response.
Exposure to prenatal maternal stress, or prolonged separation from mother in rodents
and non-human primates, can result in lifelong changes in HPA stress response (Mac-
cari et al., 2003; Meaney 2001; Suomi, 1997; cf. Levine, 2005). Research on the de-
velopmental pathways has targeted the homeostatic mechanisms of the HPA system,
which appear sensitive to exposure to high levels of glucocorticoids during ontogeny.
Glucocorticoid receptors (GRs) in the hippocampus that are part of the negative feed-
back loop regulating release of CRH and ACTH can be damaged by the neurotoxic
levels of cortisol associated with traumatic events (Sapolsky, 1990b, 2005). Hence
early trauma is posited to result in permanent HPA dysregulation and hypercorti-
solemia, with consequent deleterious effects on the hippocampus, thymus, and other
key neural, metabolic, and immune system components (Mirescu et al., 2004; Zhang,
Parent, Weaver, & Meaney, 2004). These effects have additional consequences result-
ing from high density of GRs in the pre-frontal cortex in primates (DeKloet, Oitzl, &
Joels, 1999; Patel, Lopez, Lyons, Burke, Wallace, & Schatzberg, 2000; Sanchez,
Young, Plotsky, & Insel, 2000).
Finer-grained analysis of the epigenetic mechanisms involved with maternal ef-
fects on glucocorticoid negative feedback on CRH release indicates that DNA methy-
lation affects hippocampal GR exon 17 promoter activity (Weaver et al., 2004). The
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 51
18
24
9
0
57
FIGURE 4. Children exposed to early family trauma in utero or post-natal have higher
average (means for each child) cortisol levels at ages ten and above than children who
were not exposed to early trauma (no EFT). Sample sizes (# of children) are in bars.
Vertical lines represent 95% confidence intervals. Figure adapted from Flinn, 2006b.
permanence of DNA methylation, set during a sensitive period in the first week after
birth in the rat, is a mechanism connecting diminished maternal care (e.g., licking,
grooming, and arched-back nursing) with long-term elevations of HPA stress response.
The specific mechanisms affecting relations between exposure to trauma early in
development and subsequent HPA system function in humans are not as well docu-
mented as in animal studies. Nonetheless, a similar causal linkage appears plausible
(e.g., Essex, Klein, Cho, & Kalin, 2002; Heim et al., 2000; Lupien et al., 2005;
O’Conner, Heron, Golding, Glover, & ALSPAC study team, 2003; Teicher, Andersen,
Polcari, Anderson, Navalta, & Kim, 2003). Children in the Bwa Mawego study who
were exposed to the stress of hurricanes and political upheavals during infancy or in
utero do not have any apparent differences in cortisol profiles in comparison with chil-
dren who were not exposed to such stressors. Children exposed to the stress of
parental divorce, death, or abuse (hereafter “early family trauma” or EFT), however,
have significantly higher cortisol (Figure 4) levels at age ten than other children. EFT
children also have higher morbidity than non-EFT children (Flinn, 2006b). Based on
analogy with the non-human research discussed previously, two key factors could be
involved: (1) diminished hippocampal GR receptor functioning, resulting in less ef-
fective negative feedback regulation of cortisol levels; and (2) enhanced sensitivity to
perceived social threats, perhaps as a consequence of lower social competencies. Chil-
dren usually elevate cortisol in response to strenuous physical activity, but rapidly re-
turn to normal levels (Figure 5). If EFT has affected the negative feedback loop, then
recovery to normal cortisol levels would be slower. Resumption of normal cortisol
levels after physical stressors, however, appears similar regardless of early experience
of family trauma (Flinn, 2006b). Cortisol profiles following social stressors, however,
52 MARK V. FLINN AND DAVID V. LEONE
.75
Cortisol (µg/dl)
.50
.25
0
7:00 AM 12:00 PM 5:00 PM
indicate that EFT children sustain elevated cortisol levels longer than non-EFT chil-
dren (Flinn, 2006b).
The enhanced HPA stress response of children in this community that were ex-
posed to EFT appears primarily focused on social challenges, suggesting that the on-
togenetic effects of early trauma on stress response may be domain-specific and even
context-specific. These results are consistent with studies of the effects of social de-
feat with non-human models (e.g., Kaiser & Sachser, 2005). In the following section
we examine the effects of close grandparental relationships on the stress response of
EFT children.
1.0
Cortisol (standardized)
FIGURE 6a. EFT children with high grandparental care (GPC) have lower average
cortisol levels than low GPC EFT children. Vertical lines represent 95% confidence
intervals.
10
% days ill, (standardized)
1.0
0
Controls EFT children EFT children
(N = 57) w/high GPC w/low GPC
(N = 28) (N = 23)
FIGURE 6b. EFT children with high grandparental care (GPC) have lower average
morbidity levels than low GPC EFT children. Vertical lines represent 95% confidence
intervals.
(Figure 6d) or lower gastrointestinal parasite loads (Figure 6e) than EFT children with
low GPC. These results suggest that grandparental care may substantially ameliorate
some of the negative consequences of difficult family environments. These findings
are generally consistent with our subjective impressions from watching these children
over nearly two decades: that grandparental relationships are often of great importance
54 MARK V. FLINN AND DAVID V. LEONE
50
Growth percentile
40
FIGURE 6c. EFT children with high grandparental care (GPC) have higher average
growth percentiles than low GPC EFT children. Vertical lines represent 95% confi-
dence intervals.
Fluctuating asymmetry (%)
2.5
2.0
FIGURE 6d. EFT children with high grandparental care (GPC) do not have lower lev-
els of fluctuating asymmetry (FA) than low GPC EFT children. Vertical lines repre-
sent 95% confidence intervals.
for the development of emotional regulation, social skills, and self-confidence, espe-
cially for children in difficult family environments. What the specific mechanisms are,
and whether the effects are direct or indirect via support to the child’s mother, are not
discernable from these analyses.
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 55
40
Parasite loads (%)
20
FIGURE 6e. EFT children with high grandparental care (GPC) do not have lower lev-
els of parasite loads than low GPC EFT children.
Conclusions
Grandparental care appears to be a significant mediator of HPA stress response and
associated growth and health problems among children that have experienced early
family trauma. Our observations suggest that maternal grandmothers are especially
important mediators, (Quinlan & Flinn, 2005), although a variety of other kin (e.g.,
aunts, siblings, grandfathers) may also contribute, and in special cases, may be pri-
mary caregivers (Flinn & Leone, 2006). These results are likely to be specific to the
context of the kin networks of this community (e.g., see Quinlan & Flinn, 2003), and
are likely to vary contingent on the specific patterns of kinship, although grandparent-
grandchild relationships appear to be broadly important (Lahdenpera et al., 2004; Sear
et al., 2000; Voland & Biese, 2002). These results are consistent with the hypotheses
that the importance of grandmothers in human evolution may involve their role as
providers of social information (e.g., emotional comfort, social competencies, tradi-
tions) (Coe, 2003) in addition to providing calories and protection (Alexander, 1974;
Hawkes, O’Connell, Blurton Jones, Alvarez, & Charnov, 1998).
Returning to the paradox of why natural selection favored sensitivity of stress re-
sponse to social stimuli in the human child, several points emerge. Human childhood
is a life history stage that appears necessary and useful for acquiring the information
and practice to build and refine the mental algorithms critical for negotiating the so-
cial coalitions that are key to success in our species. Mastering the social environment
presents special challenges for the human child. Social competence is difficult because
the target is constantly changing and similarly equipped with theory of mind and other
cognitive abilities. Results from the Dominica study indicate that family environment,
including care from grandparents, is a primary source and mediator of stressful events
56 MARK V. FLINN AND DAVID V. LEONE
in a child’s world. The sensitivity of stress physiology to the social environment may
facilitate adaptive responses to this most salient and dynamic puzzle, aided by infor-
mation and security provided by effective parental and grandparental care.
Children lacking such care may be at a disadvantage in developing the social com-
petencies necessary for coping with social challenges, and consequently may be at in-
creased risk for problems ranging from dysregulation of emotional control and in-
creased risk of psychopathology (Gilbert, 2001; Nesse, 1999), to broader health issues
associated with social and economic disparities (Adler, Boyce, Chesney, Cohen, Folk-
man, Kahn, & Syme, 1994; Dressler et al., 2005; Marmot & Wilkerson, 1999). The
potential for intergenerational cycles that perpetuate social relationships that affect
stress (Belsky, 2005; Belsky, Jaffee, Sligo, Woodward, & Silva, 2005; Fleming, Krae-
mer, Gonzalez, Lovic, Rees, & Melo, 2002; Fleming, O’Day, & Kraemer, 1999; Fran-
cis, Diorio, Liu, & Meaney, 1999; Maestripieri, Lindell, Ayala, Gold, & Higley, 2005)
and poor health are especially concerning. Under such circumstances, grandparents
helping their grandchildren cope with difficult events involving their parents, inter-
vening during times of critical need and stabilizing development, may be of critical
importance (e.g., Lussier, Deater-Deckard, Dunn, & Davies, 2002).
We are still far from identifying the specific mechanisms linking stress response to
the ontogenetic plasticity of components of the limbic system and pre-frontal cortex
that are involved with the acquisition of social competencies. An evolutionary devel-
opmental perspective can be useful in these efforts to understand this critical aspect of
a child’s world by integrating knowledge of physiological causes with the logic of
adaptive design by natural selection (Worthman, 1999). It reminds us that our biology
has been profoundly affected by our evolutionary history as fundamentally social
creatures, including, perhaps, a special reliance upon grandparents. Indeed, the mind
of the human child may have design features that enable its development as a group
project, guided by the multitudinous informational contributions of its ancestors and
co-descendants. Children without grandparental input may find themselves in worlds
that are more stressful because they lack the advice, traditions, good humor, soft laps,
and hugging arms by which to understand them.
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The Development of Spontaneous Gestures
in Zoo-living Gorillas and Sign-taught Gorillas:
From Action and Location to Object Representation
Joanne E. Tanner
Scottish Primate Research Group, and Collaborator,
Centre for Social Learning & Cognitive Evolution, School of Psychology
University of St. Andrews, Scotland
Francine G. Patterson
The Gorilla Foundation/Koko.org
Woodside, California
Richard W. Byrne
Centre for Social Learning & Cognitive Evolution,
Scottish Primate Research Group, School of Psychology
University of St. Andrews, Scotland
rwb@st-andrews.ac.uk
Introduction
Research in recent decades has shown that zoo-living apes create gestures other than
the obviously species-typical, and signing apes regularly employ signs that they have
themselves created, in addition to taught signs. We explore the relationship of sponta-
neous gestures by zoo-living gorillas to those created by a sign language-taught gorilla.1
1. In this paper we will use the word “sign” for human sign language taught to apes, and also for gestural in-
ventions by signing apes. “Gesture” refers to inventions by zoo gorillas.
69
70 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
Particular attention is given to the development of iconic gestures because they re-
quire a type of understanding that can be linked to human representational abilities.
Here we define an iconic sign or gesture simply as one that depicts a physical aspect
of its referent. Zoo-living gorillas use iconic gestures for actions anticipated or desired
(Tanner & Byrne, 1996, 1999); in both species of chimpanzee as well, iconic gestures
have been observed both in untaught captives (Kohler, 1925; Yerkes, 1943; Hayes,
1951; Savage-Rumbaugh, Wilkerson, & Bakeman, 1977) and chimpanzees trained in
symbol systems other than sign language2 (Savage-Rumbaugh, 1986; Greenfield &
Savage-Rumbaugh, 1990, Savage-Rumbaugh & Lewin, 1994). Signing apes also cre-
ate novel iconic signs; unlike zoo captives, they spontaneously create signs to repre-
sent objects for which they have not been taught signs, and use such invented, un-
taught signs repeatedly and consistently (Gardner & Gardner, 1971; Patterson, 1980;
Patterson & Cohn, 1990; Miles, 1978, 1993; Miles, Mitchell, & Harper, 1996). The
usage of iconicity can be traced in the chronological development of gestures in indi-
vidual gorillas, and the forms the iconicity takes and what it represents are important
keys to understanding ape cognition.
We survey signs Patterson and Cohn (1990) list as invented by Koko during her first
ten years of sign language instruction, with particular attention to those that appear to
be iconic, and we note the types of iconicity that Koko uses and make comparisons with
zoo gorillas’ gestures. We assess modes of representation in terms of their order of ap-
pearance in Koko’s individual development, and compare the developmental progres-
sion and age of appearance of similar gestures in zoo gorillas. We consider the spatial
media in which gestures and signs are produced. We compare the usage of those ges-
tures or signs that take the same form in both zoo gorillas’ and Koko’s usage to learn
whether their “meanings” or functions are universal or variable. Though the gestures of
gorillas have not been extensively studied by other researchers until very recently,
where possible we incorporate any relevant data from other gorillas in zoos or the wild.
Subjects
Only two gorillas have been extensively taught a human sign language: Koko (a
zoo-born female lowland gorilla) and Michael (a wild-born male lowland gorilla, now
deceased). Koko resides at the Gorilla Foundation in Woodside, California. Koko was
born at the San Francisco Zoo on July 4th, 1971, and is the full sister of Kubie, a prin-
cipal subject of the first author’s zoo observations. Koko’s exposure to American Sign
Language (ASL) and constant interaction with human companions began at the age of
one year under the tutelage of the second author, Francine Patterson, who was at the
time a graduate student at Stanford University. Koko was simultaneously exposed to
a variant of American Sign Language and human (English) speech. Further detail of
the education of gorillas Koko and Michael and the entire ongoing project can be
found in Patterson (1978, 1979, 1980), Patterson & Linden (1981), Patterson & Cohn
(1990), Patterson & Gordon (1993, 2002), and Bonvillian & Patterson (1993, 1999).
2. Because the researchers working with these apes do not describe their gestures in physical detail, they can-
not be compared with those of signing apes or apes not taught a symbol system.
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 71
Information regarding the gestures of zoo-living gorillas is drawn primarily from
Tanner & Byrne’s long-term study of the gorilla group at the San Francisco Zoo (Tan-
ner 1998, 2004; Tanner & Byrne 1993, 1996, 1999). See www.gorillagestures.info for
video examples of the San Francisco Zoo gorillas’ gestures and more about the re-
search on the gorilla group there. From 1988 until 1997 observations were made out-
doors at the San Francisco Zoo one morning each week for approximately three hours,
conditions permitting. Further observations, on a less regular basis, have continued
until this writing. The study team consisted of the first author and the camera opera-
tor, Charles L. Ernest. The general procedure was to videotape all social interaction
continuously wherever it was possible to use the video camera. Later, videotape was
analyzed and gestures were cataloged into a Filemaker™ database. As a working def-
inition, the term “gesture” applied to all discrete, non-locomotor limb and head move-
ments that appeared to be potentially communicative, regardless of receptive sensory
modality.
The subjects, the gorillas at the San Francisco Zoo, are members of a stable social
group; all of them have spent nearly all of their lives at this zoo. The San Francisco
Zoo’s present gorilla enclosure has been this group’s home since 1980. It has an out-
doors area of 2300 square meters, or 38 by 50 meters at maximum parameters. It is
covered with grass and other vegetation and contains large, climbable live trees as
well as several dead trees, large stumps, and two artificial rock hills including arches
and cave-like areas.
The group at the time of the beginning of the study included first- and second-
generation descendants of the wild-caught founder, Bwana, who had been at the zoo
since 1958. A wild-caught female, Pogo, human-reared in her early years, grew up at
the zoo with Bwana and is of about the same age. Two young females whose early
rearing was by humans in zoo nurseries, Bawang and Zura, joined the group in 1981
and 1982 respectively, after the deaths of two older females. Bawang is the mother of
Kubie’s offspring, Shango, Barney, and Nneka, who have all been mother-reared.
Bawang was always Kubie’s preferred mate, but when she was pregnant or involved
in caring for her first infant, Kubie switched his attentions and play activity to the
younger female, Zura. All of these gorillas have been subjects of the Tanner and Byrne
studies, but the interaction between Kubie and Zura received the most intense analy-
sis; by far the greatest amount of gesturing was done by these two gorillas.
3. Two sets of criteria were used: the Emitted criterion accepted as a vocabulary item each use of a recogniza-
ble sign used spontaneously in an appropriate context; the Patterson criterion accepted a sign only if it was observed
and recorded by two different observers to be used appropriately and spontaneously on at least half the days during
a period of a month. By the end of ten years, Koko had acquired 876 words by the Emitted criterion, 290 words by
the Patterson criterion. The spontaneously invented signs discussed in this paper all met the Emitted criterion.
72 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
iconic signs decreased, though it remained higher than that of the human children stud-
ied by Bonvillian and Patterson (1993). Bonvillian and Patterson, however, acknowl-
edge that the design of their study does not allow us to discern the influences from hu-
mans on the content of taught sign vocabulary. Also some taught iconic signs may
represent aspects of the referent that would not be recognized by the learner as iconic.
Here we will look only at signs that were created by the gorillas that were not part of
their taught American Sign Language vocabulary.
In summarizing the first ten years of Koko’s vocabulary development, Patterson
and Cohn (1990) list Koko’s entire vocabulary during these ten years and indicate
which of those signs were not taught, but used spontaneously by the gorilla. These
spontaneous creations were not a result of deliberate human reinforcement of chance
novelty; untaught signs were often not initially comprehended by Koko’s human com-
panions and were ignored or misunderstood until repeated context made the meaning
clear. Thus Koko’s untaught signs can be expected to be free from human influence in
choice of referents. In some cases, the inventions were for actions, objects, or concepts
for which Koko had not been taught a sign; others were for actions, objects, or con-
cepts for which she had been taught a sign but for which she strongly seemed to pre-
fer her own usage. Once acknowledged by humans as part of her vocabulary, untaught
signs were neither discouraged nor encouraged, but simply accepted as part of Koko’s
repertoire of signs. (It is, of course, possible that humans have failed to understand and
interpret some of Koko’s signs. Also, because iconic signs are easier for us to attempt
to translate, they might be over-represented in summarizing Koko’s vocabulary.)
We categorize, according to type of iconicity or other form of reference, fifty signs
that Patterson and Cohn (1990) characterized as “invented” by Koko. This was done
with the help of an unpublished, internal-use video created by Dr. Francine (Penny)
Patterson and Darlene Chan for Gorilla Foundation employees, unpublished lists of
Koko’s sign lexicon, published physical description of earliest signs (Patterson, 1978),
as well as the first and second authors’ personal experience and knowledge of Koko’s
signing. Not included are those listed as “natural” (Patterson & Cohn’s term for signs
or gestures they suspected to be species-typical) or “modulated or compounded”
(modulated means modifying the taught articulation of a sign; compounded means
combining aspects of taught signs to form a new sign). The total corpus of 50 signs,
with descriptions and categories, is included as an appendix. Table 1 summarizes the
referential categories of Koko’s untaught signs, and Table 2 their types of iconicity or
other modes of depiction. Plate 1 illustrates some of Koko’s untaught signs.
Of Koko’s untaught signs during the first ten years of her life, approximately half
represented objects and another third, actions (Table 1). Three-quarters of her un-
taught signs involved an iconic mode of depiction (Table 2). Among these, approxi-
mately 70% involved depiction of action, either of an action itself or of a customary
action upon an object. Though these untaught signs were predominantly signs for ob-
jects, more than half of these objects were not represented by depicting their shape,
but by an action performed upon or with them. For instance, modeling clay was signed
by a motion of rolling the palms together, as when rolling out clay; a hand puppet by
74 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
the motion of putting the puppet on the hand. Some action mimes listed as represent-
ing objects might seem to be just as well translated as signs for actions, not for ob-
jects. However, Koko often used them to request the object in question (by accompa-
nying pointing or reaching with eye contact), thus indicating that an object was the
referent of the action.
In some cases the signs might be interpreted either way; in American Sign Lan-
guage, many signs can represent either an object or an action depending on repetition
and other differences in production. An action can refer to an object, and an object de-
piction may be part of an action request. Also, the categories of action and object de-
piction are not necessarily mutually exclusive because it is possible to indicate a shape
and also an action in a single sign. An example is Koko’s sign for dental floss, where
Koko picked her teeth with an index finger (untaught), and then made the taught sign
for thread, which traces the shape of dental floss.
About 40% of Koko’s untaught iconic signs represented an object by depicting an
element of the shape of the object. Since it is usually impossible to represent the en-
tirety of an action or an object with the hands, a salient aspect must be chosen to rep-
resent it. Such condensation of depiction is an aspect of both ape and human signing.
Koko’s specific choices of forms of metonymy, i.e., representing an object or action by
depicting just a part of it, will not be the focus here though well worthy of further
study. (A description of the form of each untaught sign can be found in the Appendix.)
Here we consider metonymic signs simply as iconic. Because our primary interest
here is the cognitive processes leading to the physical representation, we consider a
sign that describes any part of the physical form of an action or object to be the result
of some kind of process of iconic representation. Koko’s means of representation are
discussed in detail later in the section entitled “Koko’s Modes of Invention.”
Some of Koko’s untaught signs were not iconic. One was a deictic (pointing) sign
that indicated the location of an object (Koko’s early “notice” sign, glossed as bird at
the time because she co-opted elements of this taught sign and used it in a deictic man-
ner). Another sign simply located a referent on the self (e.g., body hair indicated by
grasping hair between the fingers). Koko also created signs that involved cross-modal
transfer of English sounds to a sign;4 for instance, blowing forcefully at someone to
express that they “blew it,” that is, performed an action she wasn’t pleased with (she
was quite familiar with the colloquial expression, frequently used in the spoken En-
glish of her companions, often to scold her). In this case, the “sign” is itself a sound,
accompanied by characteristic body posture and facial expression. Some inventions
were “blended” from several taught signs (e.g., apricot = the sign for peach made with
an “A” hand shape like apple). A few were of unknown or indiscernible origin (like
Koko’s lip in reference to human females, performed by rubbing an index finger hor-
izontally on her lips).
4. A study of Koko’s response to alterations in vowels or consonants in spoken words illustrated that Koko
can accurately perceive the sounds of human speech (Goodreau, Patterson & Tam, 1996; Patterson & Goodreau,
1987; Goodreau, 1987).
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 75
Another frequent element of Koko’s untaught signs, as well as of taught signs she
has altered to her personal preference, is locating them on her body as opposed to
forming them in space away from the body. Of her untaught signs, 60% were placed
on the body location of the referent.
Michael, Koko’s male gorilla companion, also used untaught signs, and Koko sub-
sequently adopted some of these for her own use. Untaught signs originated by
Michael but co-opted by Koko during the first ten years of the project were hit-in-
mouth, hit-in face, and pull-out-hair, all mimes of the described actions.
5. There have also been some observations in the wild, such as those found in Schaller (1963) and Robert
Campbell’s unpublished film for Dian Fossey at the National Geographic Society (viewed in entirety by the first
author), that can give us an idea of at what stage mountain gorillas in their native environment make certain kinds
of gestures.
76 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
Table 3. From Actions to Objects in Gesture and Sign Invention: First Appearances of
Different Kinds of Representation.
Signing
gorilla, age
What Zoo, wild in years and
sign or gorillas, months
gesture Example earliest age when first
describes or How Where (English Physical observed used or
indicates produced formed gloss) description to be used invented
location touch on an object knock fist contacts object zoo age 7 knocks, age
indicated to location (other than such as rock or tree; 1 but not to
other self or other eye contact and indicate
gorilla) response waiting to location to
other gorilla other
that index finger or fin-
gers contact object not seen 1.0
location extend in space that, there index finger not seen 1.0
indicated to finger extended from hand
other toward toward location
location
action upon enacted in space up arms raised to zoo age 1; 1.0
self desired request or anticipate wild infant
from other being picked up by
adult
action enacted non- on other’s move away light push to other’s zoo age 2; 1.0
desired of forcefully body body wild adults
other
action mimed on own tickle index strokes under- not seen 1.2
desired of body arm or sole of foot
other
action traced on body of turn around on other’s waist, arm zoo age 7 1.11
desired of other moves from one side
other of body to other
object hand shape, on own bracelet, cupped hand pats not seen 2.8
location body hand puppet wrist
action traced in space away, go arm swept toward zoo age 6; 2.9
desired of other wild all ages
other
action upon enacted on own bite biting self on hand zoo age 7; 2.10
other body or wrist wild
anticipated juvenile
object action on or with hands clay flat hands, top hand not seen 3.8
of an object in space in moves back and
mimed front of forth over other palm
body
negation altering on own Frown manipulate face zoo age 7 4
facial body (KOKO)
expression cover up face with
hide play- hands
face (ZURA)
object tracing of on own eyeglasses index fingers trace not seen 6.1
shape of body lines from eyes to
object back of ears
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 77
Table 3. (Continued)
Signing
gorilla, age
What Zoo, wild in years and
sign or gorillas, months
gesture Example earliest age when first
describes or How Where (English Physical observed used or
indicates produced formed gloss) description to be used invented
location on touch move arm in armswing arm swings from zoo age 7 6.4
self location space, to under space in front of
indicated to location on (walk up body to between legs
other own body bottom)
object formed by in space pickle thumb and index not seen 7+
static hand extended from both
shape only fists held in space
in front of body
object tracing of in space thread two little fingers not seen (used only
shape of touch then move when taught
object apart horizontally by humans)
Observations of gestures in the wild come from the following sources, but primarily the publications
of George Schaller and Dian Fossey: Baumgartel, 1976; Burbridge, 1928; Campbell unpublished
film; Denis, 1963; Fay, 1989; Fossey, 1979, 1983; Mori, 1983; Schaller 1963/1976, 1964.
Sources: Patterson (1980); Patterson, Tanner & Mayer (1987); Patterson & Cohn (1990); Tanner (1998)
Arranged chronologically by order of appearance in signing gorilla.
firm one, as learning and genetics are so entwined for any behavior and further, since
we do not have good observations of behavior for all groups of gorillas, especially in
the wild. A better designation, which we use throughout, is simply between human-
taught and untaught signs.
Koko’s earliest recorded untaught signs were listed as “natural” signs, though her
standard deictic sign, pointing with the index finger, has not been reported in untaught
gorillas. Further untaught signs seen early in the first year of instruction (age 12–24
months) were up, requesting an action upon the self by another; and tactile signs such
as a light push to another, indicating move away. By the end of the year a tactile sign
using a tracing motion on another’s body appeared, requesting a companion to turn
around.
Gorillas at the San Francisco Zoo have been observed to use all the “natural” un-
taught gestures performed by Koko in her first year of sign instruction, except for point-
ing with the index finger. Later in development knock or pound (using the fist) and slap
(open hand) are used by zoo gorillas to touch objects in a clearly deictic fashion, with
eye contact and waiting for response from the partner gorilla.6 Such usage was ob-
served repeatedly in a 7-year-old gorilla and her older play partner but may appear ear-
lier; Tanner’s zoo observations began when the younger of her principal subjects was
already age 7. Subsequent observations of younger zoo gorillas by Tanner and others
6. See Leavens, Hopkins, & Bard, (1996), Leavens & Hopkins (1998, 1999), for discussions of variability of
form in pointing by chimpanzees. The development of pointing in human children and the criteria for social
pointing have been discussed by many scholars, for instance Butterworth (1996) and Bates, Benigni, Bretherton,
Camaioni, & Volterra (1979).
78 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
(Pika, Liebal, & Tomasello, 2003) did not find such referencing, however. Likewise,
tactile gestures on another’s body, requesting directional movement of the other gorilla,
were rarely seen in zoo gorillas until age 7.7 Miming on the gesturer’s own body of the
specific action desired of another was not observed at all in zoo gorillas.
The earliest untaught signs recorded as invented by Koko are blow and tickle,
which depicted actions desired of another and appeared during her second and third
months of sign instruction, when she was just over a year old. The earliest appearance
of blow was putting her index finger to another’s mouth when the person stopped blow-
ing, perhaps simply pointing; Koko appeared to want the person to continue blowing.
Koko then began to request the action “blow” by holding a finger up to her own mouth,
transferring the features of another’s body to her own. Tickle was likewise indicated by
miming the action desired of another on her own body. Her next sign was a deictic sign,
performed with two index fingers held together at the tips. This sign was directed to-
ward interesting objects out of reach, but was glossed bird because it incorporated el-
ements of a bird sign a teacher first used. Subsequently, however, Koko employed it
for many referents other than the bird the teacher had originally been pointing out.
Koko’s next type of untaught sign did not appear until over a year later, during
which time her taught ASL signing progressed rapidly. This sign, at age 2 years 8
months, was bracelet, performed by a cupped hand patting the wrist, first used request-
ing a new bracelet she was shown. This was her first sign created for an object, and in-
volved an iconic hand shape depiction as well as contacting the part of her own body
where the object usually was worn, thus perhaps involving a tactile element as in ear-
lier signs such as tickle. She later extended the use of the bracelet sign, referring to a
hand puppet on a companion’s hand as well as using the sign for bracelets. This seems
to be an extension of the ability to point out location to another, which Koko did at the
age of just one year. It is requesting “something on my body, wrapped around this lo-
cation.” A zoo gorilla (Kubie) comes close to this in a unique observation when he pats
his shoulders, with eye contact, in interaction with another gorilla (Zura), resulting in
her approaching Kubie and placing her hands on his shoulders (Tanner & Ernest, 1989).
Koko’s next untaught sign, bite, appeared at age 2 years 10 months (see Plate 1).
She placed the side of her hand or index finger in her mouth to request biting play
from a companion. A similar gesture has been observed in both free-living and zoo ju-
venile gorillas and the first author has observed it in captive monkeys where a play
partner was not physically available. Like Koko’s earliest untaught signs, bite repro-
duced the action desired of another, on her own body. Around the same time, another
untaught sign, away or go, appeared. It differed from the earlier sign, up, in that it de-
picted in space motion desired from another, not motion anticipated for the self. A sim-
ilar gesture was used by zoo gorillas from age 6, and has been seen in the wild.
At age 3 years, 8 months, a new type of depiction appeared: Koko’s sign for clay.
Koko requested clay by miming the customary action performed on the object, rolling a
7. Tactile gestures consisting of reaching, stretching and touching are seen early on (also in gorillas studied
by King, 2004) but not tracing a path of action or suggesting motion in a certain direction as found in older go-
rillas by Tanner and Byrne (1999).
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 79
ball of clay between the hands. This could be interpreted as depicting the activity of play-
ing with clay rather than the object itself, but Koko used such signs to request objects.
During Koko’s first five years, all her iconic inventions reproduced action of or upon an
object, or objects were indicated by simply placing an appropriate hand shape on her
body. No signs depicting an object or its action have been observed in zoo gorillas.
At age 6 years a new mode of depiction appeared for Koko: tracing the shape of
an object. Koko created a sign for eyeglasses where index fingers traced a line from
the eye to the back of the ears. Eventually, Koko produced a total of 15 inventions de-
scribing objects that involved depicting the shape rather than the action of an object
(see Appendix). A form of active “tracing” of the form of an object was used in five
cases; in ten cases, her depictions of shape were produced instead by a descriptive
hand shape (e.g., extended finger for a straight or narrow object, cupped hand for a
rounded object, index and thumb extended for a small rectangular object) placed on
an appropriate body location. Among Koko’s 50 inventions from her first 10 years
(listed in Appendix), all signs that depicted an action were performed on appropriate
body locations, and nearly all that depicted a shape were also performed touching her
body. An exception was her later invention at age 7 of a sign for pickle (described in
Table 3), with appropriate hand shapes in the space in front of the body. The only cat-
egory of object representation not found among Koko’s untaught signs during her first
ten years is the tracing of an object in space away from the body, though she uses such
signs when taught. (Thread, a taught sign used in her untaught compound sign for den-
tal floss, is such a sign).
Also between age 6 and 7, Koko produced a sign glossed walk-up-bottom, request-
ing her male gorilla companion to touch or tickle her bottom. A similar gesture was
frequently observed in zoo gorillas, described as armswing under. For the zoo goril-
las as for Koko, this gesture appeared in adolescence. For the zoo gorilla Kubie, this
often included a tap to the other gorilla, and then swinging the arm to a location be-
tween the legs. His version actually was a phrase that can be glossed as “you come
under,” that is, a request to make contact with the gesturer gorilla’s genital area.8
To summarize, the chronological development of modes of representation in
Koko’s spontaneously created signs is as follows:
1) (from age 1–2 years) depicting actions on her own body, another’s body, or in
space, to represent activity desired of another; and pointing to objects or loca-
tions desired or noted
2) (from age 2.8) placing the hand-shape of an object on an appropriate body lo-
cation, to represent an object or action
3) (from age 3.8) miming an action performed with or on an object in order to
represent an object
4) (from age 6) tracing on her body the outline of an object to describe the object
5) (from age 7) tracing a shape in space away from the body or using a hand
shape held in space away from the body to describe an object
These last two were the rarest of Koko’s means of representing objects, though
these methods of depiction are common in American Sign Language and are em-
ployed in many of her taught signs.
she began to take sexual interest in a human visitor not amongst her caretakers, a lab-
oratory worker who wore heavy boots, and it has been speculated that Koko was using
the boots as a point of reference; this visitor also sometimes played a game tickling
Koko’s foot, and she may have extended her foot to him then. There is another possi-
ble derivation, however. A gesture observed several times in the zoo female Zura (see
Table 4), consisted of turning the rear toward and extending a foot back to another go-
rilla, a mounting reference possibly derived during development from a signal com-
monly used by a mother for a youngster to get on her back. Zura sometimes tapped
the sole of her extended foot with her index finger as part of this signal, sometimes
only tapping the foot without presenting the rear, in the context of sexual play. This
tap foot is identical to Koko’s “man” (foot) sign, which Koko used frequently in the
context of human men, but not, for instance, for a “family” member such as her “sur-
rogate father” Ronald Cohn. If the derivation suggested is correct, it would be an ex-
ample of an adaptation of a “natural” behavior to a new context.
Untaught signs created by Koko after her first ten years have not been formally de-
scribed in academic publications but many are described in articles in the Gorilla
Foundation’s semi-annual Journal. Signs now regularly glossed as above and below,
whose meaning at first eluded researchers, have become a standard part of Koko’s
repertoire (Patterson & Tanner, 1988). These depict spatial location by moving a flat
palm forward off the top of the head (above) or moving a flat palm from between the
legs when seated (below).9 Another sign noted only in recent years has been glossed
as take-off, referring to removal of clothing, lifting both flat hands quickly off the top
of the head. Koko has also continued to transfer sounds of human speech into signed
form, as in her frequent sign for vegetable browse (see Plate), a term for which she
was not given a sign. The spoken word was not used until a change in diet when
browse items of leafy green vegetables began to be distributed to Koko at intervals
throughout the day. Koko makes the browse sign by placing a fist (“S”-hand) on her
brow, with the tapping motion of the sign for “lettuce” from American Sign Language
(Menendez & Patterson, 1994).
As well as inventing signs for referents for which she had not been provided with
an ASL sign, Koko replaces some of her taught signs with untaught ones for the same
referent, perhaps because her own versions are more meaningful to her when clearly
iconically related to a referent or touching her body. Also, as previously noted, she
seems to prefer signs without intricate hand configurations, substituting signs easier
for gorilla hands to articulate, and signs that touch her body. An example is her usage
(a cross-modal transfer) of knee (tapping a finger on her knee) for “need,” for which
she had a taught sign; the ASL version of need is performed with a crooked index fin-
ger moving downward in the open space in front of the body. Another untaught sign
that makes use of gorilla anatomy is Koko’s exaggerated version of frown, using
her hands to pull her lower lip down rather than simply tracing downward lines at the
corner of the mouth as in the ASL sign. In many ASL signs she retains the motion and
place of a sign but changes or simplifies hand shape; in some she retains motion and
9. This depiction of the concept that something is located below something else seems to be a directional re-
versal of Koko’s walk-up-bottom sign and Kubie’s frequent armswing under gesture.
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 83
hand shape but changes the place, usually to her body or a surface in her environment
such as wall or floor.
General Discussion
A gorilla tutored in sign language and gorillas living in a zoo both create signs or
gestures that depict and invite action and point out objects and locations, but signs that
refer to objects themselves are invented only by the signing gorilla. Many of the un-
taught signs of signing apes and the gestures of non-signing apes have iconic charac-
teristics. Iconic descriptions can be formed in several different ways, depending on
what aspect of an action or object is chosen as salient, i.e., what kind of metonymy is
employed. Gestures describing similar actions or objects, therefore, may vary within
and between different groups of apes (Tanner, 1998). On the other hand, some gestures
or signs that are physically very similar are shared between signing and non-signing
apes but may not have the same functions; these may be iconic gestures that are sim-
ilar in appearance because they describe similar material, or may be hitherto little
known species-typical gestures elicited by a relevant social environment (see Table 4).
84 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
armcross (glossed as catch) used in activi- play contexts; function otherwise zoos and
ties involving tossing and catch- unknown wild
ing of objects; chase games,
playing hard to get; also request-
ing embrace or desirable objects
armshake (glossed as play or hurry) play invitation, readiness for activity; SF Zoo,
invitation to play; also expression sometimes warning or threat (only not in
of excitement or impatience used this way by one individual) wild
armswing under (glossed as walk-up-bottom) invitation for contact in sexual play SF Zoo,
sexual solicitation or request for not in
tickling of bottom wild
away (glossed as stop) to stop advance agonistic contexts, avoidance of zoos and
of another individual contact wild
backhand (glossed as darn) expresses gaining attention in play situations, zoos and
annoyance or frustration also used in agonistic display or wild
protest
bite in playful excitement, referring in play, before or after biting play zoos and
to biting wild
chestbeat excitement, agitation, but also in excitement, agitation, attention zoos and
a more controlled form glossed getting wild
as gorilla
circle hands (glossed as gentle) request for unknown, but seen in play contexts zoos and
gentle behavior wild
clap playfulness or excitement in play, often solitary and before zoos and
performing a physical action like wild
jumping or balancing
deictic (pointing) (glossed as me, you, that, there, designating other or self as object or zoos and
gestures your) designating numerous agent of action; also designating loca- wild
referents and locations; Koko tions. Performed with open hand,
performs points with extended knuckles or fist. Glossed as chest fist
index finger. Your is performed pat, tap other, pound, extended palm
with outstretched palm, may
designate another’s property or
turn for action.
extended palm (glossed as come-gimme) invitation to contact or request for zoos and
(could be included requesting objects or the food wild
with deictic gestures) approach of other individuals
facewipe (glossed as toilet, b.s.) expression annoyance, avoidance SF Zoo
of disbelief, uncertainty or
annoyance
foot designating the body part, also seen in a zoo gorilla, a variation of one SF
referring to human males foot back sexual invitation performed Zoo
by tapping the foot with the hand gorilla
hand between legs (glossed as below) performed play, sexual invitation (usually patting SF Zoo,
seated; hand moving out from motion) Rio
under body designates location Grande
below or under another object. Zoo
When forceful slapping motion, a
masturbation activity.
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 85
Table 4. (Continued)
Koko’s untaught Koko’s usage Where
signs also observed with Gorilla Usage at observed
in other gorillas Foundation gloss San Francisco Zoo (zoo, wild)
hands behind back (glossed as walk-up-back) inviting play activity or approach zoos
requesting companions fingers from companion seated behind self
walked up back, tickling
head nod (glossed as yes) agreement, inviting approach or visual attention one SF
assent of other gorilla Zoo gorilla,
wild
head shake, head (glossed as no) dissent head shake used in playful contexts; zoos and
turn head turn sometimes avoidance wild
or possible request for change of
direction
knock, pound attention getting, or cross-modal get visual attention in playful context; zoos and
(fist hand shape) transfer of English “obnoxious” indicate location or direction wild
slap surface (for Koko, glossed as pound) play or chase invitation zoos and
(flat hand) play invitation of challenge; wild
referential use to request attention getter
pounding on her back
tactile gestures indicate movement desired from indicate movement desired from an- zoos and
another by non-forceful contact other by non-forceful contact or mo- wild
or motion upon other’s body; can tion upon other’s body; can take
take many different forms: can many different forms: moving hand
take many different forms: mov- down back vertically or across hori-
ing hand down back vertically zontally, patting, gentle pulling of
or across horizontally, patting, hand, light push away, and others
gentle pulling of hand, light push
away, and others
up for movement upward; request to request or intention to move upward zoos and
be picked up wild
Observations of gestures in the wild come from the following sources, but primarily the publications
of George Schaller and Dian Fossey: Baumgartel, 1976; Burbridge, 1928; Campbell unpublished
film; Denis, 1963; Fay, 1989; Fossey, 1979, 1983; Mori, 1983; Schaller 1963/1976, 1964.
(Koko’s usages from Patterson, 1980; Patterson & Tanner, 1988; zoo data from Tanner, 1998)
The fact that some of the gestures performed by signing apes resemble those of
apes in the wild has been seized upon by some as evidence that apes do not really learn
human sign languages, but only perform gestures that they would “naturally” use any-
way (Pinker, 1994; Wallman, 1992). The accumulation of evidence does not support
contentions that signing apes do not really use sign language but only adapt their
species-typical gestures. “Natural” or species-typical gestures are indeed used by
symbol-taught apes, but they may often elaborate upon them and have opportunities
to use them in a greater variety of contexts than do apes in the zoo or in the wild. In
addition to such species-typical gestures, apes with different upbringings are likely to
invent gestures similar to each other’s, given a common ability for iconic representa-
tion, similar anatomies, and similar material to describe. In addition, signing apes, of
course, use a large vocabulary of taught standard sign language in addition to species-
typical gestures and untaught signs. Even when modified by anatomy of the ape hand,
86 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
much of this signing is nothing like their “natural” gestures. Few gestures resembling
American Sign Language signs are spontaneously formed by untaught apes, who use
a limited number of hand shapes compared to apes taught ASL.10
The iconic gestures a signing gorilla creates are more numerous and elaborate than
those of zoo captives, probably because of intensive exposure to symbolic modes of
communication and interaction with humans. Early input may alter brain utilization in
humans (for instance, a heightened sense of pitch in humans blind since infancy,
Gougoux, Lepore, Lassonde, Voss, Zatorre, & Belin, 2004) and no doubt in apes (Bard
& Vauclair, 1984; Povinelli, 1994). A recent experiment with marmosets (South Amer-
ican monkeys) showed that in only one month, those monkeys housed in larger and
more enriched environments actually developed denser neuron growth and had more
of the synaptic proteins the brain uses in relaying messages between neurons, in con-
trast to control subjects housed in minimal caged situations (Kozorovitskiy, Gross,
Kopil, Battaglia, McBreen, Stranahan, & Gould, 2005).
Where great apes have been shown to possess capacities once reserved for hu-
mans, such as the ability to imitate goal-directed actions and understand their reflec-
tion in mirrors and employ referential pointing, the apes have often been individuals
raised by humans (discussions of the strong claim that human-rearing “enculturates”
apes, giving them human capacities they do not naturally develop, are found in sev-
eral chapters in Parker, Mitchell, & Boccia, 1994). Skills salient in humans would be
likely to be more utilized in apes with a good deal of exposure to humans (Povinelli,
1994; Gomez, 2004). Iconic representation is, after all, related to imitation in that it is
a form of mime, and requires the taking of another’s perspective when depicting an
action or object outside the self as well as kinesthetic/visual matching (Mitchell, 1994;
Byrne, 1995). Expressing, in iconic fashion, action desired from another appears rel-
atively late in Koko’s inventions (age 2) and even later in zoo gorillas’ development
(age 6–7). Request for another’s action upon the gesturer’s own body appears earlier.
Gestures requesting action of another require understanding of the other as an inde-
pendent agent and also an understanding of the other’s point of view. For instance, the
gorilla must have an awareness that the visual attention of the partner is necessary for
communicating with gestures; such understanding was present in the adolescent zoo
gorillas studied by Tanner and Byrne (and in younger gorillas; see Gomez, 1990,
1991, 1994, 1996).
Koko moves further than zoo subjects with her untaught signs: from depicting so-
cial action, to use of a “still” image to represent an object, to reproduction of custom-
ary behavioral action upon an object to represent that object, then to tracing the out-
line of an object. Thus there is a transition from pure behavior and “intention
movements” to representation of proposed action from others (rather than one’s own
action), and finally to non-action representation of objects.
Signing apes and zoo captives have in common action and location as the most
prevalent descriptive elements used in forming their gestural creations, even those un-
10. American Sign Language has nineteen primary hand shapes plus twice as many variations; a deaf human
child untutored in sign language created nine hand shapes (Goldin-Meadow, 1984). Untutored gorillas seem per-
haps to have three: open palm, fist, and knuckle hand.
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 87
taught signs of the gorilla Koko that represent objects. This may be because of the go-
rilla’s limited comfort with the intricate hand shapes utilized in human sign language
that would more precisely describe object shape, but are not suited to gorilla anatomy.
Alternatively, however, preference for action as a descriptive mode may be related to
cognitive processing. The brain has specialized cells for visual reception of hand and
limb movement that respond strongly to hand-object interactions (Perrett et al., 1989).
More recently neurons termed mirror neurons have been found to react to actions per-
formed on objects, but do not react to an object alone, or to the same action performed
without an object involved (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; Rizzolatti,
Fadiga, Fogassi, & Gallese, 1996; Rizzolatti & Arbib, 1998; see Rizzolatti & Craig-
hero, 2004, for a review of mirror neuron research, and Roy & Arbib, 2005; Arbib,
2002, 2005, regarding implications for language production and perception). Most re-
cently, research has shown that the understanding of others’ manual actions is influ-
enced by context (objects nearby) that implies what the subject’s intention might be
(Iacoboni, Molnar-Szakzac, Gallese, Buccioni, Mazziotta, & Rizzolatti, 2005). The
implication that actions are understood through their context and that objects are un-
derstood through the actions performed on or with them aligns well with the fact that
the majority of Koko’s untaught signs for objects were made by portraying a custom-
ary action associated with the object.
Within the framework of the function of mirror neurons, Arbib provides a scenario
that neatly parallels the progression we have found in moving from zoo gorillas’ spon-
taneous gestures depicting action, to Koko’s inventions for objects. Demonstrating
how bridging from action to language could take place, Arbib (2002) provides a hy-
pothetical sequence for development of gesture in evolutionary history that moves
from pragmatic action towards a goal object, to imitation of such actions (required in
order for Koko to establish an iconic sign for new objects/actions), to pantomime pro-
duced away from the goal object (what Koko does when establishing a new sign in her
vocabulary, getting the observer to focus on a specific action, or an object associated
with it). The next stages Arbib posits are: abstracting gestures from their pragmatic
origins, which is what happens when Koko makes a (metonymic) choice of what as-
pect of action to use to henceforth represent the target action or object; then using the
new sign in compounds with other previously established taught or untaught signs, as
she does. Koko presumably jumps up to the latter phases, not found in zoo gorillas or
other untaught apes, because her enculturation with human communication enhances
her understanding of shared attention and conventions of language.
The predominance of descriptive action in untaught signs may be biologically fa-
cilitated by the mirror neuron system; proximately, it may be due to the fact that it is
through shared action that social discourse takes place between gorilla and gorilla, or
gorilla and human companion in Koko’s case. For Koko, the introduction of a new and
unfamiliar object like a stethoscope or modeling clay would be meaningless without
a demonstration of the usage of that object, and it is that usage that makes the object
come alive as a part of the shared interaction involving it.
In Koko’s development, actions were depicted earlier than hand-shape object
descriptions, and tracing of outlines of objects was latest to appear. Tracing a shape is
88 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
cognitively very close to drawing or writing (as noted by Edwards, 1979). Koko is
able to paint depictions of objects that are correctly placed in their relative spatial and
size locations and to select appropriate paint colors, but her paintings are not always
detailed in reproduction of shape (for a photograph of a painting and its model see Pat-
terson, 1985).11 Because the tracing of shapes for Koko seems to be most comfortably
and extensively performed on the surface of her own body, there might also be a tac-
tile element involved in some of her signs; the hand shape for glasses, for instance,
might involve a tactile memory of touching the frames of glasses on one’s head, or for
scarf, the feeling of a scarf covering her head. Koko, in her learned ASL signs, was
taught numerous signs for objects that were not touchable, or could not be touched by
her: examples might be clouds, sun, tree, and house. These signs, however, are not
among her most frequent spontaneously used vocabulary items.
Though a tactile element is part of many of Koko’s untaught gestures, some of
these signs apparently originate from transfer of a visual feature observed on someone
else onto herself, as in her sign for filmers/reporters (tracing the outline of the straps
seen on camera bags). Transferring features observed on someone else to one’s own
body is rather like touching oneself on a location observed in a mirror. For humans,
feeling that one is actually tracing the outline of an object in a tactile manner when
putting it on paper has been shown to produce accurate and natural artistic depictions,
even by those with no artistic training; most people, however, instead perform the in-
termediary step of mentally representing, or visualizing, an object to oneself and only
after this drawing it on paper (Edwards, 1979). In the zoo gorillas, tracing of motion
on another gorilla’s body is a frequent medium of requests for action. This tactile
propensity, born from physical interaction, may underlie many of the inventions of
both the zoo gorillas and Koko. The model object was present when Koko first cre-
ated her “shape tracing” signs, but she also used them later in the absence of the orig-
inal model, implying memory of either the shape of the object or her previous actions.
Gorilla gestures, both of zoo and signing gorillas, seem to arise from an under-
standing of paths of action that can be tactile, visual or locomotor. Underlying the ges-
tural abilities of all great apes is the anatomical characteristic of rotational movement
of the joints, a characteristic that humans share, derived originally as an adaptation to
brachiation under tree limbs and arboreal “clambering.” The locomotor adaptations
permitting brachiation in apes allow a much greater flexibility of limb control than
possessed by monkeys, which potentially has consequences for all manual activities
(Morbeck, 1994). Several theories have been put forward that specifically relate ape
cognition to demands of the physical environment (reviewed in Byrne, 1997). Parker
and Gibson (1977, 1979; see also Bard, 1990) propose that seasonal foraging, on foods
that require extraction from a matrix, selected for tool-using propensities and abilities.
Povinelli and Cant (1995) (see also Chevalier-Skolnikoff, Galdikas, & Skolnikoff,
1982, p. 643) propose that arboreal clambering, by an animal too large to risk a fall,
selected for the ability to imagine itself in a detached, objective way and thus plan safe
routes through the canopy, dealing with constantly changing conditions in transferring
11. Chimpanzees and other apes have also painted; for a most extensive illustrated discussion, see Morris,
1961, and Hoyt’s (1941) early description for the gorilla Toto.
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 89
from tree to tree. Orangutans use supports that are flimsy relative to their weight much
more often than do monkeys in the same habitat, and use multiple supports, whereas
monkeys prefer single supports. On this theory, viewing the self as an object led to the
ability in apes to recognize their own selves reflected in a mirror.
Both the extractive foraging and complex locomotion accounts focus on a single
modern species (the tool-using chimpanzee, the arboreal clambering orangutan) as
models of the common ape ancestor, making them difficult to test against comparative
data. Byrne (1997, 1998, 2000, in press) proposes that feeding competition from sym-
patric monkeys—smaller animals with lower metabolic needs, more efficient long-
range travel, and ability to eat less ripe fruit—selected for skills in manual foraging,
allowing apes to exploit foods unavailable to their competitors, such as insects within
mounds or trees, and plants defended by spines or stings. All modern apes feed in
ways that are manually skillful compared with monkeys, involving complex, hierar-
chically organized techniques that are unlikely to be invented by a solitary individual
(Byrne, 2002). Critical to skill acquisition, then, is the ape’s ability to decipher the
skilled manual actions of others and thereby learn novel techniques (Byrne & Rus-
son,1998; Byrne, 2003; Whiten, Horner, de Waal, 2005). Behavior parsing and hierar-
chical program-building abilities, functioning to allow apes to exploit a wider range
of foods by allowing traditions of skill to accumulate by social learning, have been ex-
plicitly related to the origins of gestural communication (Byrne, 2000, in press).
Building up hierarchically structured action-plans, from simpler building blocks of
actions in the ape’s extensive manual repertoire, is seen as the evolutionary origin of
the syntactic structuring of language components. However, none of these theories
deals specifically with the iconic abilities that have been a prominent focus of the
present analysis. Iconic gestures are anticipations of action, including actions of oth-
ers as well as anticipated or previously experienced actions of the agent itself, that the
gesturing gorilla must be able to represent mentally and then express through a kind
of mime. Moreover, the gorilla is apparently able to translate between different scales,
expressing desired large-scale body movements of others by using the smaller com-
pass of its own hand gestures.
We propose that action mapping in three-dimensional space is an important capa-
bility of all great apes. Action mapping can be defined as the mental ability to picture
motion in space, predict its results before performing it, and translate from the large-
scale of real world motions of bodies (whether observed, remembered, or anticipated)
into the smaller scale of hand movements that iconically describe them. The capacity
to map seamlessly from observed bodily motions to corresponding actions of the self
appears closely related to the “active intermodal matching” theory, proposed by Melt-
zoff & Moore (1977) (Meltzoff, 1996) to underlie the ability of very young children
to copy the facial gestures of adults. They suggest that humans are born equipped with
the ability to match their own muscular movements with the movements they see oth-
ers make, a 1:1 system of correspondence that bridges across modalities. The action
mapping concept also is supported by the existence of mirror neurons and their func-
tions, as discussed earlier. In a communicative context, as in gorilla gesturing, action
mapping would mean mentally picturing motion in space and its possible results (ei-
ther on the basis of memory or anticipatory planning) and then performing it, without
90 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
the need for any step-by-step shaping process. In communication, action in real space
can be “miniaturized,” mapped in hands or arms.12
Though it seems that many gestures may be mapped directly to the hands from ac-
tion in the real world, some form of imitative process is often posited as a way in which
novel communication might be propagated. Let us look at the evidence for imitation, or
any kind of social learning, of gestures. Frans de Waal describes the spread of a behav-
ioral tradition in captive chimpanzees (de Waal & Seres, 1997). The capacity to repro-
duce nonfunctional limb motions demonstrated by a human in a “do as I do” task has
been shown in captive chimpanzees (Custance et al., 1995) and also in gorillas (Byrne
& Tanner, 2006 in press). Orangutans imitate elaborate human activities, sometimes in-
volving a series of several actions (Russon & Galdikas, 1993), and imitation at a pro-
gram level seems to be the best explanation for the complex, hierarchically-organized,
and highly plant-specific feeding techniques seen in mountain gorillas (Byrne & Byrne,
1993; Byrne & Russon, 1998). For gorillas raised in a signing environment, imitation
of a human’s signs is a frequent way of learning new signs, even in a gorilla not for-
mally taught signs. Ndume, an adult male gorilla brought to the Gorilla Foundation to
be a companion to Koko, was never formally taught any sign language, but began grad-
ually to use some of the same signs that Koko and her gorilla companion Michael had
been taught, and to compound signs (Patterson & Gordon, 2002; Patterson, 2005).
At the zoo, some evidence speaks against imitation as a way of learning gestures.
Many of the gestures shared by all the gorillas in the San Francisco group are gener-
ally accepted as species-typical. The use of a few gestures by some but not all mem-
bers of the group remains unexplained. The gesture armshake, for instance, is not seen
in all gorillas, though it has been recorded at several zoos and was used by several
members of the San Francisco Zoo group. Kubie’s son, Shango, who at an early age
watched many of the play sessions between Kubie and Zura during which armshake
was frequent, never developed armshake as a part of his gestural repertoire, and it has
only very rarely been observed in his mother, Bawang. On the other hand, Shango’s
younger brother Barney armshakes frequently and seemed to move from, in earliest
observations, using armshake in a solitary way, to using it socially. Pika et al. (2003)
found some gestures that were widespread among members of one zoo group studied,
but not found at all in another group elsewhere. Stoinski (2006) in a survey of goril-
las in different zoos found that numerous behaviors, including gestures, varied consid-
erably from zoo to zoo, indicating each zoo had its own set of potentially cultural
behaviors.
Another indication of gorillas’ capacity to remember and reproduce actions comes
from the observation of repeated sequences of actions, gestural and otherwise, by go-
rillas in the San Francisco Zoo group (Tanner, 1998), in contexts of play and display.
Though they involved the reproduction of a gorilla’s own previous actions, not those
of another, these sequences show that the memory capacity necessary for reproduction
of complex activities is available for the gorilla. Ability to reproduce complex se-
quences of functional activities makes sense in the action mapping context.
12. Gestures in adults are miniaturized in comparison to those of young children (McNeill, 1992).
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 91
The work of Tomasello and colleagues posits ontogenetic ritualization, a process
of fading or shaping frequently performed actions in repeated interactions with an-
other individual, as the main process through which ape gesture is created (Tomasello,
Kruger, Farrar, & Evans,1985; Tomasello, Gust, &, Frost, 1989; Tomasello, Savage-
Rumbaugh, & Kruger, 1993; Tomasello, Call, Nagell, Olguin, & Carpenter, 1994;
Tomasello, 1999 for an overview). The adaptive explanation of action mapping is a
simpler one than ontogenetic ritualization, which as a process has been deduced but
never actually observed in full. In the experience of the present authors, ontogenetic
ritualization is not a completely satisfying explanation of all inventions by zoo goril-
las or by signing gorillas. Instead, much invention appears to begin not with shaping
of a functional action directed toward another gorilla, but with one of these two
processes: (1) a spontaneous natural body movement (perhaps a sign or gesture such
as armshake) is expanded or altered when re-used in varying situations of social inter-
action, eventually gaining meaning through repeated interactions, or (2), an iconic
movement is produced by putting into manual motion an action mentally anticipated
or desired. For Koko, this, with manual reproduction of shapes of objects as well as
actions, was the primary method of invention. Such gestures or signs, generated by ei-
ther process, may vary in scope, size, and dynamic according to context, as do signs
in human sign languages. Type (1) invention is not entirely removed from the idea of
ontogenetic ritualization though it need not begin with a functional action; type (2),
however, would be generated by action mapping without any need for a ritualization
process. Koko’s gestures, above, below and browse, discussed earlier in this paper
were all spontaneously used by the gorilla well before human companions understood
them, thus no shaping process could exist. In the zoo, Barney’s usage of armshake ap-
peared to develop from spontaneous use of an idiosyncratic, but anatomically feasible
movement, used at first in a solitary context and only later developed in social con-
texts. It is also not impossible that the two kinds of gesture creation described above
could both be used in forming one meaningful gestural motion, though an example has
not been found at present.
Pointing and other deictic gesture is not well explained by ontogenetic ritualiza-
tion. There are too many variations in size, scope, location, and orientation of gestures
indicating locations for each gesture to be likely to be individually ritualized. Like-
wise, though zoo gorillas’ tactile iconic gestures may appear to be “faded” from force-
ful actions, new gestures constantly appear in different directions and dimensions,
with no two exactly alike. It is unlikely that each gesture would be individually faded.
Many untaught gorilla gestures combine action mapping with the deictic principle of
locating a sign appropriately in a certain location, on one’s own body or on another’s
body. An example from zoo gorilla Kubie, come shoulders, involved patting both his
shoulders with his palms, to which play partner Zura responded by approaching and
placing her hands on his shoulders (Tanner & Ernest, 1989). Koko also early gener-
ated an untaught “pointing” sign. The taught sign “bird,” used by her instructor to
point out a bird seen through the window was co-opted by Koko as a sign for various
animals and novel objects on the other side of the window. Koko used both index fin-
gers to point in a configuration similar to the original sign performed by the instruc-
tor, an extended thumb and index finger.
92 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
At the San Francisco Zoo, Kubie used his established repertoire of gestures with
several gorillas and was later understood by new individuals. He used most of the
same repertoire of gestures he used with Zura in his interactions with two other fe-
males in the group during other time periods years apart. His most frequent gestures
were all used regularly over a period of more than seven years, though proportions of
the different gesture types used with each female varied. Apparently different recipi-
ents were able to interpret his actions and the resulting interactions were favorable
often enough that it benefited each new pair to establish such communication. Action
mapping as a cognitive ability shared by apes explains this mutual understanding of
iconic gesture between different partners without any need for re-shaping.
Thus, though gorillas in the zoo group varied in their repertoires of gestures, with
some gestures being shared with other gorillas, and others unique to individuals, the
gorillas still seemed to have developed a mutually understood system of communica-
tion. This was particularly striking in Kubie and Zura’s interactions; their gestures
often alternated in a turn-taking conversational manner and seemed to be used to make
decisions about type, timing, and location of play as well as simply promoting contact
(Tanner, 2004).
Koko’s untaught signs for objects are unlikely to be explained as “faded” from ac-
tion, but they can be understood as formed by an ability to map and mirror visual input
with the hands. Ontogenetic ritualization “takes two” to shape gestures for mutual in-
teraction, but originating a sign for an object does not require interaction for its inven-
tion, only to establish it as a mutual communicative element. Shared cognition and
shared backgrounds along with shared interaction with objects, make understanding
of such signs possible. Koko’s newly untaught iconic signs thus eventually make good
sense, once decoded by human companions.
Because anatomy and behavior evolve in interaction with the environment, the
contexts in which gestures most frequently take place are important in understanding
what their ultimate function might be. The gestures observed in zoo gorillas were at
their highest frequencies in play and quasi-sexual situations, and pygmy chimpanzees
(also known as bonobos) in captivity used iconic gestures to settle on copulatory po-
sitioning (Savage & Rumbaugh, 1977). Further, Crawford (1937) saw the spontaneous
emergence of much gesturing in an artificial context where two chimpanzees had to
cooperate and coordinate their movements in order to receive food rewards. Signing
chimpanzees, when observed through remote videotaping with no humans present,
conversed with signs and gestures about play, grooming, and other social matters but
hardly at all about food and eating or discipline and dominance (Fouts & Fouts, 1989).
What all these situations of rich communication have in common is the necessity of
coordination of movement around the environment, or cooperation in movement. The
term co-regulation in the manner of Alan Fogel’s mothers and children could just as
well be applied (Fogel, 1993). Visual and tactile gestures proliferate when mainte-
nance of close contact with another, or closely coordinated movement, is necessary for
interaction to be successful (King, 2004).
Gestures and signs also obviously thrive when an environment is vested with con-
specifics and objects with which interaction is desirable and pleasurable; Greenspan
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 93
and Shanker (2004) describe the importance of function and emotion and how com-
plementary they are in the development of communication. In a study of the pragmatic
functions of Koko’s signing during her first year of instruction (between age 1 and 2
years), the categories found to be used by human children were all used by Koko;
these included labeling, repeating, answering, requesting action, requesting an answer,
calling, greeting, and protesting (Patterson, Tanner, & Mayer, 1988). A glance at the
list of Koko’s inventions (Appendix) shows that her untaught signs were for things
and activities in her environment that Koko was interested in, but for which she had
not been taught a sign. She needed signs in order to maintain shared attention with her
companions, and so generated ones of her own invention. In some cases, her signs
were emotional comments, such as her unlisten, unattention, frown, and blew-it signs.
Koko and her gorilla companion Michael’s sign acquisition has been compared to
that of signing human children in several studies by Bonvillian and Patterson (1993,
1999). Similarities were found in type of vocabulary content, acquisition of referen-
tial signing, and in the generation of various non-sign gestures. Differences were
found in rates and patterns of early language and gestural milestones, with gorillas
reaching many of these milestones but at a slower rate than children. The same could
be said for the zoo gorillas in comparison to the sign-instructed gorillas. Comparison
of the untaught signs of Koko, a signing gorilla, and gestures of zoo gorillas shows a
continuum of representation, where a signing gorilla moves further than the zoo goril-
las along a line that proceeds from behavior directed at immediate goals, to represen-
tation of desired action, to representation of objects.
Gesture may well be the structural foundation upon which language is built, and
we can find in gesture the thread of evolutionary continuity between animal action and
human language (King, 1999; Byrne, in press). The present study shows that it is
likely that in the history of our hominoid ancestors, the earliest iconic depictions were
of action rather than objects, just as we find in apes. Because such iconic capacity is
present in gorillas, and surely in orangutans, given their related ability to imitate and
to use human sign language (Russon & Galdikas, 1993; Miles & Harper, 1994; Miles
et al., 1996; Shapiro & Galdikas, 1995), it was most likely present 10 million years
ago in the common ancestor of hominoids. New means of communication, when they
occurred in our ape ancestors, would certainly have achieved increased success for in-
dividuals in social, and ultimately, sexual relationships. Such behavior would surely
have selective value, and over generations result in gestures becoming increasingly
frequent and complex. Through the condensation of real activity to something repre-
senting it, in forms progressively more removed from the original, hominid commu-
nication have, over millions of years, reached the arbitrariness that is a characteristic
of human language. But not all of human language even today is purely arbitrary. We
can still see glimpses, particularly in sign languages, of the development of language
from the raw materials of action (Armstrong et al., 1995). The creation and usage by
gorillas of special repertoires of gestures gives us a window into the developmental
processes and environmental pressures that might have led an ancestor ape to further
refinement of iconic communication, and its eventual expansion to human gestures of
the mouth.
94 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
Credits: The authors wish to thank Barbara King, Christa Nunes, and two anonymous
reviewers for their time spent reading this paper and for their helpful suggestions. The
first author wishes to thank Charles L. Ernest, her husband, for his video documenta-
tion since 1988 of the San Francisco Zoo gorillas and their gestures, as well as contin-
ual technical support of all kinds.
Appendix
Koko’s untaught signs: first 10 years
(Signs from Patterson & Cohn, 1990, analysis of iconic characteristics by first author)
Key:
O: object
A: action
D: deictic
IS: iconic for shape of object
IA: iconic for an action
BL: indicates (self) body location of referent
BLO: on body of other person or gorilla
CMT: cross-modal transfer from English sounds
D: deictic; pointing
U: unknown derivation
FA: functional action
Gloss in English Physical form Type of iconicity or Kind of
and classification of untaught sign other type of reference representation
apricot “A” hand shape with motion like cross-modal transfer from CMT
O “peach” sign (hand brushed English sound as well as
down cheek) compounding signs
barrette index finger draws line forward draws shape of object, also IS, BL
O above ear where barrette is usu- places on body location
ally placed
bird (notice) index fingers, held together at deictic D
D tips, point to location of object
of interest that is out of reach
bite teeth bite index finger side of iconic for action IA
A hand
blew-it loud exhalation: blowing sound cross-modal transfer from CMT
A directed at offending person English sound
blow blows on index finger held verti- iconic for action IA
A cally in front of mouth
body hair fluffing up hair on the body by indicating part of body BL
O rubbing both hands up and down
on body
bracelet cupped hand encircles and pats iconic for shape of object, IS, BL
O wrist placed on body location
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 95
clay palms together, move back and iconic for action, on cus- IA, BL
O forth in circular rolling motion tomary body location
dental floss pick index on teeth plus thread iconic for shape and action, IA, IS, BL
O sign (two little fingers touch on body location
then move apart horizontally)
drip-chin mime with index the action of iconic for action, on body IA, BL
A liquid rolling down chin location
dripping index imitates motion of drip- iconic for action IA
A ping liquid on cheek
earphones thumb and index of both hands iconic for shape of object, IS, BL
O move down body from ears placed on body location
eye makeup index finger strokes horizontally iconic for action, placed on IA, BL
O across eyelid body location
fake-sneeze imitates sound and motion of iconic for action IA
A sneezing
fake-tooth taps upper or lower rear tooth body location BL
O with index
fang tap lower canine teeth with iconic for shape of object, IS, BL
(Halloween toy) hooked index fingers placed on body location
O thumb and index of both hands iconic for shape of object, IS, BL
filmers, reporters move down body where camera placed on body location
O straps are located
frown lower lip pulled down over chin iconic for shape, placed on IS, BL
O with fingers body location
glasses thumb and index pinch at iconic for shape of object, IS, BL
O temples placed on body location
grate imitating motion of grating a iconic for action IA
A vegetable; fist moves across
palm of other hand
hair bow index and thumb of both hands iconic for shape of object, IS, BL
O placed on head placed on body location
inhale index from mouth down to iconic for internal path of IA, BL
A stomach an action in body
kiss-hand kiss on hand iconic for action IA
A
long hair index fingers trace hairline from iconic for shape of object, IS, BL
O ears to below shoulder placed on body location
man, male (foot) taps bottom of foot with index unknown U
O
nail file tip of bent index moves back and iconic for action, placed on IA, BL
O forth across finger of other hand body location
96 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
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102 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
Peter G. Roma
Department of Psychology
American University
Angela M. Ruggiero
National Institute of Child Health and Human Development
Stephen J. Suomi
National Institute of Child Health and Human Development
Abstract: Behavioral interactions and infant stress reactivity were investigated in 120
mother-infant pairs of rhesus monkeys (Macaca mulatta). The mothers themselves were ei-
ther mother-reared (MR), surrogate-peer reared (SPR), or peer-reared (PR). Focal obser-
vations and isolation stress tests were conducted throughout post-natal months 1–6 of the
infants’ lives, followed by a standardized 4-week social separation regimen. PR mothers
engaged in more grooming than MR mothers during months 4 and 6, and more rejections
than both other groups during months 3 and 5. Although all infants were mother-reared,
D 14 and 30 cortisol responses in infants of MR and SPR mothers resembled their mother’s
responses at that age, a pattern that corresponded inversely with levels of mother-infant
mutual ventral contact during month 1. Despite observed differences in maternal behav-
ior and evidence of non-genomic cross-generational transmission of early cortisol reactiv-
ity, infant stress responses throughout later infancy did not vary as a function of the
mother’s rearing condition.
103
104 PETER G. ROMA, ET AL.
Method
Subjects
Data were analyzed from a total of 120 mother-infant pairs of rhesus monkeys
(Macaca mulatta) collected over eight consecutive birth-year cohorts; the infant sub-
ject pool was composed of 74 males and 46 females. All mothers and their infants were
group housed in combined indoor-outdoor pens with another 6–8 adult females from
the same cohort as each other and with their infants from the same cohort as each other.
106 PETER G. ROMA, ET AL.
Each group also included two adult males who sired their respective group’s infants.
All animals had ad libitum access to water and monkey chow with regular supplements
of fresh fruit and grains. All procedures described in this report were in compliance
with the Animal Welfare Act (1966) and Public Health Service Policy, and all proto-
cols were approved by the NICHD and NIAAA Animal Care and Use Committees.
between 0900 hr and 1600 hr. The behaviors of interest for our study were: Grooming
between mother and infant, Mutual Ventral contact between mother and infant, Social
Contact between mother and infant, and Reject/Withdrawal between mother and in-
fant. The operational definitions and scoring criteria for these behaviors are outlined
in Table 1 (the entire mother-infant ethogram is available upon request).
and olfactory, but limited visual and no tactile contact. At one hour post-separation,
each infant was removed from its holding cage and another blood sample was taken
(H1); after this sampling, the infants were returned to their respective holding cages.
Finally, a third blood sample was taken two hours post-separation (H2) in the same
fashion as the H1 sampling. The Baseline, H1, and H2 blood samples were taken while
the monkeys were fully awake, and provided the opportunity to assess acute stress ef-
fects on HPA axis activity. Following the H2 sampling, the infants were returned to
their holding cages where they remained for three days. On day 4, each infant was
anesthetized (15 mg/kg ketamine, IM) followed by blood and CSF sampling (H96); the
H96 sampling provided the opportunity to assess the impact of a chronic stressor on
HPA axis output. On D5, the infants were reunited with their mothers in their respec-
tive home groups, where they remained for three days. Following the 3-day reunion
period, the 4-day separation and 3-day reunion sequence was repeated until a total of
four full cycles was completed over the course of 28 days.
All blood samples were kept on ice until centrifugation (within three hours after
extraction), after which the plasma was transferred to cyrotubes and immediately
flash-frozen in liquid nitrogen. Samples were then stored in a –80° C freezer until
shipped for assay. Levels of plasma adrenocorticotropic hormone (ACTH) and total
cortisol were determined via radioimmunoassay by a commercial assay facility; inter-
and intra-assay coefficients of variation were ≤ 10%. ACTH values were expressed in
picograms per milliliter (pg/ml) and cortisol values were expressed in micrograms per
deciliter (µg/dl).
Data Analyses
Most of the infants studied were reared by multiparous mothers over successive
years; specifically, the 120 infant subjects were reared by 78 different mothers. Of the
120 infants, a total of 57 (47.5%) were reared by primiparous mothers, whereas a total
of 75 infants (62.5%) were reared by females who were or would later become multi-
parous. Maternal parity notwithstanding, the data from each mother-infant pair were
considered independent of each other; therefore, each dyad was treated as an inde-
pendent case for analyses. Data were analyzed using Analyses of Variance (ANOVA),
paired-samples t-tests, planned least-significant difference (LSD) between-groups
comparisons, and Pearson product-moment correlations as described in detail below.
Statistical significance was set at α = .05 for all analyses (2-tailed when applicable).
Individual Differences
A number of studies from the animal literature have demonstrated clear relation-
ships between individual differences in early maternal behavior and subsequent stress
reactivity in offspring. The best known and most widely reproduced relationship is the
negative one between licking/grooming behavior in rat dams (Rattus norvegicus) and
subsequent neuroendocrine responses to stress in their pups (see Meaney, 2001). How-
ever, individual differences in maternal care among nonhuman primates are regularly
observed (Fairbanks, 1996; Maestripieri, Lindell, Ayala, Gold, & Higley, 2005), and
in order to determine if analogous relationships existed in differentially-reared rhesus
monkey mothers and their infants, a series of correlational analyses was conducted via
Pearson product-moment correlations. Specifically, mean mother-infant grooming be-
havior during each month of each infant’s life was plotted against the infants’ corre-
sponding ACTH and cortisol values for that month. Also, to assess whether early ma-
ternal care can predict stress reactivity in later infancy, month 1 grooming behavior
was correlated with mean ACTH and cortisol responses to each phase of the separa-
tion procedure. All of the above mentioned correlational analyses were performed sep-
arately for infants of MR, SPR, and PR mothers.
110 PETER G. ROMA, ET AL.
Results
25 250
22 *#
19 200
16
150
(mean + SEM)
20
The Kids Are Alright
0.1
FIGURE 1. Mother-infant behavioral interactions as a function of mother’s rearing condition. Overall mean levels of Grooming did not
vary as a function of infant’s age; however, Mutual Ventral significantly decreased from M1-M2 and M2-M3, Social Contact increased
from M1-M2, and Rejections increased from M2-M3 and M3-M4. Each MR, SPR, and PR bar represents the respective mean of 56–57,
23, and 31–32 mother-infant pairs. Within each month, significant difference versus the MR group is indicated by *, significant differ-
111
ence versus the SPR group is indicated by †, and significant difference versus the PR group is indicated by #.
112 PETER G. ROMA, ET AL.
Infants’ ACTH
450
370
Mean pg/ml + SEM
290
210
130
50
D14 D30 M2 (Baseline) M3 M4 M5
Infants’ Cortisol
60
†
†
52 †
Mean µg/dl + SEM
44
36
*
28
20
D14 D20 M2 (Baseline) M3 M4 M5
Individual Differences
The results of the correlational analyses are summarized in Tables 2 and 3. Monthly
grooming rates were generally not associated with infant HPA axis activity at each
month; however, grooming during the first month of life was positively correlated with
D30 cortisol output among infants of MR females (r (59) = .530, p = .000016) and neg-
atively correlated with D30 ACTH output among infants of PR females (r (29) = –.491,
p = .007; all other absolute rs < .305, ps > .138). A dissociation between grooming dur-
ing the 1st month of life and infants’ subsequent responses to separation stress was also
observed, except for a modest but significant positive relationship with H2 ACTH lev-
els among the infants of SPR mothers (r (26) = .444, p = .023; all other rs < .317, ps
> .077). The statistically significant relationships between maternal care and infant
stress reactivity are presented in Figure 4.
Discussion
The purpose of this study was to explore the influence of contemporary laboratory
rearing conditions on maternal behavior in adult rhesus monkeys and to determine
how rearing effects may impact biobehavioral development in these mothers’ infants.
Given the fairly comprehensive collection of variables and the relatively large sample
size, perhaps the most striking result was the general lack of differences in maternal
behavior or infant stress reactivity as a function of maternal rearing condition. Espe-
cially in light of the original motherless-monkey work and more recent investigations
of potentially detrimental effects of nursery rearing (e.g., Barr et al., 2004; Bastian,
Sponberg, Suomi, & Higley, 2003; Higley, Suomi, & Linnoila, 1992), it is somewhat
surprising that even the mother-reared mothers failed to emerge as superior caretak-
ers, if not producers of infants with superior coping skills.
The behavioral data showed that all three groups of mothers engaged in generally
species-normative patterns of interaction with their infants, exhibiting high levels of
mutual ventral contact in early infancy, giving way to increasing levels of social con-
tact, and culminating in increased rejections as weaning approached. The most patent
deviation from the overall pattern among these behaviors was in the PR mothers’ ten-
dency to reject their 3–5-month old infants with a frequency reserved by the other two
114 PETER G. ROMA, ET AL.
Infants’ ACTH
400
330
Mean pg/ml + SEM
†
260
190
120
50
Baseline Hr 1 Hr 2 Hr 96
Infants’ Cortisol
80
70
Mean µg/dl + SEM
60
50
40
30
Baseline Hr 1 Hr 2 Hr 96
Phase of Separation
Table 3. Relationships between M1 grooming and infant HPA axis responses to separation
stress.
Relationship with M1 Grooming
Infants of Infants of Infants of
Phase of
MR Mothers SPR Mothers PR Mothers
Separation
Procedure ACTH Cortisol ACTH Cortisol ACTH Cortisol
Baseline .089 .119 .046 –.044 .182 .316
Hour 1 .123 .177 .266 .098 .143 .307
Hour 2 .048 .013 .444* .294 .172 .243
Hour 96 –.050 .126 –.023 .255 –.070 .277
Note: Each value represents Pearson r correlation coefficient. Significant correlation is bolded (p = .023).
groups for month 6. However, and somewhat paradoxically, the PR mothers also en-
gaged in more grooming behavior than their MR counterparts during the latter half of
their infants’ rearing. It is uncertain why this pattern appeared—one possibility is that
the PR monkeys’ propensity for physical contact could have provoked more rejection
responses from their MR infants as the infants grew increasingly independent—but
perhaps a more relevant question than “why?” is “did it matter?”, and at least in terms
of infant stress reactivity, our physiological data suggest that it did not.
The HPA axis data were concordant with the behavioral data in that no one group
of infants appeared particularly well- or ill-suited to cope with the isolation and sepa-
ration stress challenges. The infants of PR mothers did not differ from their MR or
SPR counterparts in HPA axis reactivity during the later months when PR mothers re-
jected their infants more frequently. In fact, infants of PR mothers involved in rela-
tively high levels of grooming during the first month of life showed relatively low
ACTH levels that month, whereas infants of high-grooming MR mothers actually
showed increased cortisol levels (see Figure 4). The former result echoes the rodent
literature if one assumes linear causality between maternal grooming and infant HPA
116 PETER G. ROMA, ET AL.
900
750
600
450
300
150
r (56) = .023, ns
0
0 20 40 60 80
Surrogate-Peer Reared Mothers
600
500
400
300
200
100
r (23) = .041, ns
0
0 10 20 30 40 50 60 70
Peer-Reared Mothers
900
800
700
600
500
400
300
200
r (29) = .491, p = .007
100
0
0 20 40 60 80 100 120
FIGURE 4. Individual differences in maternal care and infant stress reactivity. Indi-
vidual differences in mother-infant Grooming during the infant’s first month of life
served as the predictor variable for these graphs. Each column of graphs corresponds
to a different outcome variable among the infants of MR (●, n = 56–62), SPR (▲, n =
23–26), or PR (■, n = 29–32) mothers, respectively. Statistically significant correla-
tions within any combination of outcome variable and mother’s rearing condition are
indicated by an underlined graph title.
The Kids Are Alright 117
Mother-Reared Mothers
100
80
60
40
60
40
r (23) = .129, ns
20
0 20 40 60 80
Peer-Reared Mothers
80
70
60
50
40
r (29) = .396, ns
30
0 20 40 60 80 100 120
FIGURE 4. (Continued)
118 PETER G. ROMA, ET AL.
Mother-Reared Mothers
700
600
500
400
300
200
0
0 20 40 60 80
300
200
100
Peer-Reared Mothers
400
300
200
100
r (32) = .172, ns
0
0 20 40 60 80
FIGURE 4. (Continued)
The Kids Are Alright 119
axis reactivity (cf. Francis, Diorio, Liu, & Meaney, 1999); however, the latter result is
less readily explained, unless already high-reactive infants of MR mothers tended to
elicit more maternal grooming than their low-reactive peers (cf. Stern, 1997). This in-
terpretation is difficult to verify with our existing dataset, but seems reasonable given
the fact that infants of MR and PR mothers did not actually differ at the group level in
their mean D14 or D30 HPA measures.
In addition to the early grooming correlations, perhaps the most intriguing result
of the HPA analyses was the relationship between infants of MR and SPR mothers at
the D14 and D30 samplings. In their 1998 study employing the same procedures as
those we used, Shannon et al. reported significantly higher cortisol values in MR ver-
sus nursery-reared infants that were virtually identical (within 5 µg/dl) to those seen
in our infants of MR and SPR mothers (see their Figure 1 and our Figure 2 bottom
panel). The critical point here is that all of the infants in our study were mother-reared,
yet the infants of MR and SPR mothers exhibited cortisol patterns resembling those
produced by their mothers’ rearing conditions.
Since the patterns of early cortisol reactivity Shannon et al. reported were pro-
duced by the rearing conditions to which the monkeys were assigned, they cannot be
primarily attributed to genetic factors. To account for their findings, Shannon et al. ar-
gued quite sensibly that MR infants were not only subjected to the stress of the neona-
tal assessment procedure, but to the stress of capture and maternal separation, whereas
the nursery-reared infants were more acclimated to human handling and did not expe-
rience disruptive capture and separation. However, the infants in our study were all as-
signed to the same mother-reared environment, so there were no differences in proce-
dure that could account for our findings. Nonetheless, the pattern of early cortisol
reactivity in infants of SPR mothers was still identical to their own mothers and dif-
ferent from the infants of MR mothers. Taken together, these results suggest a cross-
generational transmission of early stress reactivity, but by different non-genomic
means for both acquisition in SPR mother and transmission to her MR infant.
The patterns of early stress reactivity in MR and SPR mothers can be explained by
their own differential rearing, but the identical patterns seen in their mother-reared in-
fants cannot. This point coupled with the fact that the first month of a rhesus infant’s
life is spent almost exclusively on or in very close proximity to mother leaves mater-
nal behavior as the most likely means of cross-generational transmission. Although
mother-infant grooming behavior did not vary as a function of mother’s rearing, the
SPR mothers did engage in more mutual ventral contact with their infants during the
first month of life compared to their MR and PR counterparts—a pattern that corre-
sponds inversely with the D14 and D30 cortisol data. More conclusive verification of
this relationship would, of course, require further study, but as conceptually intriguing
as these findings might be, there still remains the issue of functional consequences. As
with the behavioral tendencies produced by the mothers’ differential rearing, the ap-
parent cross-generational alterations in their infants’ early HPA axis regulation were
inconsequential when challenged later in infancy.
So overall, what can we conclude about modern laboratory-rearing effects on ma-
ternal behavior and infant stress reactivity in rhesus monkeys? Generally, it appears
that the mother-rearing, surrogate-peer rearing, and peer-rearing conditions utilized
120 PETER G. ROMA, ET AL.
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Author Note
We are grateful to Courtney Shannon, Stephen Lindell, and our many other col-
leagues and friends for their tireless efforts in data collection and management, veteri-
nary and animal care, and facilities maintenance throughout the years.
This project was supported by intramural funds from the National Institute of
Child Health and Human Development and the National Institute on Alcohol Abuse
and Alcoholism/National Institutes of Health/Public Health Service/US Department of
Health and Human Services.
Correspondence concerning this article should be addressed to Pete Roma, Depart-
ment of Psychology, American University, 4400 Massachusetts Ave. NW, Washington,
DC 20016. Email: PeteRoma@gmail.com.
The Literacy of Interaction:
Are Infants and Young Children Receiving a
“Mental Diet” Conducive for Future Learning?
Pnina S. Klein
School of Education
Bar-Ilan University
Ramat-Gan, Israel
123
124 PNINA S. KLEIN
Elements of Mediation
Basic elements of what constitutes a teaching mediational interaction between a care-
giver and a young child have been identified (Feuerstein, 1979, 1980). The most salient
of these factors are empirically defined (Klein, Raziel, Brish, & Birenbaum, 1987; Klein,
Wieder, & Greenspan, 1987; Klein, 1988, 1991) and are presented in Table 1.
It was found that the factors of quality mediation predicted cognitive outcome
measures up to four years of age better than the children’s own cognitive test scores
in infancy, or other presage variables related to pregnancy, birth histories, and moth-
ers’ education (Klein, Wieder, et al. 1987). Similar findings were reported for a sam-
ple of very low birth weight infants (Klein, Raziel et al. 1987).
Intercorrelations between mothers’ mediational behaviors over time (when their
children were 6, 12, 24, and 36 months old), were moderate to high. The average in-
terjudge reliability for assessing these behaviors was considerably high in studies of
American families of low socioeconomic status (Klein, Wieder et al. 1987) and Israeli
mother-infant samples (Klein & Alony, 1993).
Similar studies were carried out in Ethiopia, Sri Lanka, Indonesia, USA, Sweden,
and Israel (Klein, 1996). A study designed to examine the sustained effects of modi-
fying the mother-infant mediational interaction on infants’ cognitive test performance
and behavior was carried out in Israel. This study will be referred to as the Israeli
follow-up study.
The research design of the Israeli follow-up study included random assignment to
the experimental and control groups; an observational assessment of maternal media-
tion; a baseline assessment of the infants’ developmental status, using Bayley’s Men-
tal Development Scales, prior to training mothers in mediational strategies; and a
follow-up evaluation of experimental versus control mothers and children one year
and three years after the termination of training.
The total study sample consisted of 68 families in a small, low income status urban
community in Israel, who were randomly assigned to an experimental and control
group. This community was singled out for intervention by the Ministry of Education
and the Office of Welfare due to the high proportion of children who had poor school-
readiness skills and a significant high school dropout rate.
Activities developed for the experimental group were based on the Mediational In-
tervention for Sensitizing Caregivers (MISC) process, which is described in detail
later in this article. These activities were designed to improve mothers’ mediation to
their children. The level of mediation was defined by the frequency of appearance, se-
quence and synchrony of maternal mediating behaviors, and their children’s respon-
siveness. Mothers were trained at home by paraprofessional “mediators” and super-
vised by professional developmental psychologists. Mothers were actually helped to
“read” their interactions with their children, to understand their own behavior and their
children’s responses, as well as the potential consequences of these interactions.
Intervention was terminated when mothers improved their mediation and could ver-
bally define the basic components of the parental behaviors targeted by the intervention.
126 PNINA S. KLEIN
Table 1. Definitions and Examples of Basic Criteria of Parental Mediation and Affected Needs
Examples of Social-Emotional
Mediation Processes the Process Intellectual Needs Needs
1. Focusing Making the environmental Need for precision in Need to focus on and
Any act or sequence of stimuli compatible to the perception (vs. scanning decode facial and body
acts of an adult that child’s needs, e.g., bring- exploration). expressions of emotion.
appear to be directed ing closer, covering Need for precision in Need to modify one’s
toward affecting a child’s distractions, repeating, expression. own behavior or the
perception or behavior. sequencing, grouping, environment in order to
These behaviors are helping the child focus, mediate to others (to
considered reciprocal see, hear and feel clearly. make the other person
when the infant or child see or understand).
in the intervention
responds, vocally,
verbally, or nonverbally.
4. Encouraging Praise in a way that is Need to seek more success Need to please others
Verbal or nonverbal meaningful to the child. experiences. and gain more mediated
behavior that expresses Clear isolation and identi- Need to summarize one’s feelings of competence.
satisfaction with a child’s fication of the reasons for own activities and deter- Need to identify what
behavior and that identi- success. mine what led to success. pleases different people.
fies a specific component
or components of the Well timed in relation to Need to provide others
child’s behavior which the experience. with mediated feelings
contribute to the experi- of competence.
ence of success.
5. Regulating Behavior Regulation with regard to Need to plan before acting, Need to control one’s
Behaviors that model, speed, precision, force, e.g., need to consider impulses in social
demonstrate, and/or ver- and preferred sequence of possible solutions prior to situations.
bally suggest to the child activities. responding. Learn acceptable ways
regulation of behavior in Clarifying goals, meeting of expressing one’s
relation to the specific subgoals. emotions (i.e., regulate
requirements of a task, or
to any other cognitive Need to pace one’s activities. the pace and intensity of
one’s social responses to
process required prior to Need to regulate the level anger and joy).
overt action. of energy invested in any
given task.
The Literacy of Interaction 127
In the experimental group, these behaviors were represented by the criteria of mediation,
and in the control group, by basic aspects of a stimulating, responsive, non-punitive
environment.
Since mediation was found to affect children’s cognitive functioning (including
perception, elaboration, and expressive processes), it was expected that maternal me-
diation behaviors (e.g., focusing, showing affect, and expanding) would affect chil-
dren’s vocabulary and abstract reasoning and, in general, prepare children to perform
better in situations requiring “new learning,” such as tasks requiring immediate se-
quential memory. Thus, children’s cognitive performance was assessed using the fol-
lowing measures: Peabody Picture Vocabulary Test (PPVT), the auditory reception,
visual reception, visual association, auditory association, and auditory sequential
memory of the Illinois Tests of Psycholinguistic Abilities (ITPA), as well as the Beery
and Bucktanika test of visual motor integration. In addition, children’s behavior dur-
ing the play interactions with their mothers’ was video recorded and analyzed.
Comparison of the two groups on the separate components of each mediation fac-
tor, three years following the intervention, revealed that the mothers who participated
in the intervention, (i.e., learned to “read” their interactions with their children),
showed significantly more mediation behaviors (Klein & Alony, 1993).
Significant differences in favor of the children in this group were found on the
PPVT, auditory reception and auditory association measures. The average PPVT IQ for
the experimental group was 101 (SD = 15.5), and for the control group, 84 (SD = 14.1).
Of all factors of maternal mediation, mothers’ expanding and rewarding behaviors
were most frequently related to children’s cognitive performance. Within these two
types of behavior, maternal request for expansion of ideas (i.e., “Does it remind you
of anything?”, “What is it like?”) and mediation of competence with explanation
(rather than simply saying “Good,” “Fine,” etc.) were singled out as most significantly
related to the children’s cognitive performance at age four. These findings coincide
with those reported by Collins (1984), identifying the variable of “demandingness” as
one of the most essential determinants of the quality of “good” family environments.
Similarly, Heath (1983) suggests that demanding from children that they reconstruct
experiences verbally, (i.e., asking young children to tell about their experiences) may
enhance their thinking and language development. Children’s expressions of affect
were most significantly related to all criteria of maternal mediation, but mostly to ma-
ternal rewarding behaviors, maternal expansion of ideas, and maternal request for “af-
fect,” that is, attempts to arouse signs of excitement in relation to anything or anyone.
Focusing behavior in isolation from the other mediational behaviors (e.g., only
catching of attention) was not significantly related to any of the cognitive outcome
measures. A noteworthy relationship was found between the children’s performance
and the mothers’ nonverbal expression of feelings. Mothers’ expressions of feelings
were also found to be related to children’s spontaneous provision of rewards to others.
The mediational approach applied in the follow-up study was not designed to im-
prove children’s performance on specific cognitive tasks. Yet, three years following
the termination of the intervention, children in the experimental group outscored the
children in the control group with regard to language performance as measured by the
PPVT and two measures of verbal reasoning. These findings suggest that children
from poor families who participated in the intervention were brought well within the
128 PNINA S. KLEIN
about the mere survival of their family may not have enough mental energy to invest
in expressions of excitement related to objects or events in the environment or to as-
sociate those experiences with others in the child’s past or future. Thus, it is possible
that the cycle of poverty is perpetuated, since one of the types of mediation most con-
ducive to cognitive development as well as school achievement, is missing in parental
mediation to these young children.
Summary
Infants and young children require adult mediation in order to develop the poten-
tial to benefit from new experiences. Various patterns of mediation have been found
to be related to characteristic behaviors of infants and young children, reflecting the
needs to seek clarity in perception, to search for meaning, to seek information beyond
what could be perceived directly through the senses, to link between experiences
(spontaneous associations), to experience success, especially in social contexts, and
others. It is possible to enhance parents’ or teachers’ mediation through intervention,
and consequently to affect the mental development of infants and young children. Spe-
cific patterns of mediation were identified cross-culturally and in populations of chil-
dren with special needs. Learning to “read” these patterns (i.e., learning to use the lit-
eracy of interaction) may be helpful in planning suitable mental diets through quality
educational programs for young children. “Literacy of interaction” refers to sensitiza-
tion and consciousness-raising regarding key issues in the adult-child (parent-child,
caregiver-child, or teacher-child) interaction. In practice this means trying to raise the
adult’s awareness regarding his or her own basic philosophy of childrearing, percep-
tions of the child; of himself or herself as parent or teacher; of the child’s emotional
and cognitive needs; and how all these affect the interaction with the child, especially
the mediational interactions, namely the attempts to teach the child. The representa-
tion of all these components is referred to as the literacy of interaction representing a
child’s mental diet.
Most of the decisions of educational policymakers focus on what is done, rather
than on how it is done in the teaching-learning interaction. The developmental appro-
priateness of educational programs for young children is frequently assessed in terms
of outcome measures, primarily including measures of achievement, skills and abili-
ties, and rarely involving a focus on how the process of adult-child interactions poten-
tially affect children’s readiness to learn in the future. This paper suggests that answers
to the “How” question may explain much of the variability in children’s readiness to
learn, through the effects on children’s need systems, motivation, and self-regulation.
The following is an example of an educational approach exemplifying the use of the
basic ideas discussed here.
132 PNINA S. KLEIN
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grams. Washington, DC: National Association for the Education of Young Children.
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136 PNINA S. KLEIN
138
Toward a Behavior of Reciprocity 139
Now, consider reciprocity with regard to autism. The thesis of this article is that
many professionals—researchers and clinicians—and likewise many parents, have neg-
lected the reciprocal nature of reciprocity. They have forgotten that reciprocity needs to
be mutual and symmetrical—that reciprocity is a two-way street. Thus, the purpose of
this article is to move us toward a behavior of reciprocity, genuine reciprocity.
1. I have relabeled these as “cognitions” because I find it baffling that they would be considered “behav-
iors,” given that they are thoughts (e.g., awareness of what other people are thinking or feeling) or perhaps
predilections (a preference to be alone). However, such items demonstrate a type of arrogance if the observer—
the parent or teacher, who completed the questionnaire about the target child—truly believes that he is aware of
what the other person (the target child) is thinking.
140 MORTON ANN GERNSBACHER
1986). Which intervention had the more lasting influence on the autistic preschoolers’
social interaction? When the typically developing preschoolers were taught to respond
to the interaction that the autistic preschoolers initiated, the autistic preschoolers re-
sponded more frequently. In other words, when the typically developing preschoolers
behaved reciprocally, the autistic preschoolers responded more positively.
In 1988 researchers taught three autistic kindergartners to initiate pro-social physi-
cal interaction—giving high fives, patting a friend on the back—by incorporating the
actions into a song, such as “if you’re happy and you know it, give your neighbor a high
five” (McEvoy, Nordquist, Twardosz, Heckaman, Wehby, & Denny, 1988). The three
autistic kindergartners then interacted with six typically developing kindergartners, only
half of whom had also gone through the pro-social physical interaction training them-
selves. The typically developing kindergartners were considerably more likely to recip-
rocate the autistic kindergartners’ interactions if they too had gone through the training.
In 1992 researchers taught three typically developing preschoolers, called peer tu-
tors, to prompt for the verbal labels of preferred toys from three autistic children,
whom the researchers called target children (McGee, Almeida, Sulzer-Azaroff, &
Feldman, 1992). The peer tutors were told to “(a) wait for the target child to initiate a
request for (i.e., reach for) a toy, (b) ask the target child for the label of the toy (e.g.,
“Say duck”), (c) give the toy to the target child when he labels it, and (d) praise the
correct answer (‘That was great! You said duck’). None of the target autistic children
maintained their initiation with the typically developing peer tutors after the training
sessions were completed. Why not? I submit it was because the interactions were not
reciprocal. Recall that reciprocity is defined by “a relation of mutual dependence or
action or influence” and “a mode of exchange in which transactions take place be-
tween individuals who are symmetrically placed, that is, they are exchanging as
equals, neither being in a dominant position.” Peer tutors prompting autistic target
children for verbal labels is neither mutual nor symmetrical.
Given these ABA data, the following scenario related by a mother in the section
called “From the Front Line” of the near-classic ABA-for-autism manual, Behavioral
Intervention for Young Children with Autism: A Manual for Parents and Profession-
als (Maurice, Green, & Luce, 1996) makes infinite sense. The mother began by de-
scribing how she established a behavioral therapy program for her daughter.
The first order of business was to establish attending behaviors. This was ac-
complished by the therapist holding a food reinforcer at her eye level while
stating “Rebecca.” Rebecca wanted that reinforcer (a raisin or a Cheerio) so
she would look momentarily at the therapist who would immediately give her
the Cheerio and praise her verbally (Good looking, Rebecca!). Once Rebecca
began to attend, she was taught to follow simple gross motor imitations and
simple commands (stand up, clap hands, wave bye-bye). (p. 366)
By the time we hit the one year anniversary of our program 3 months ago,
Rebecca had developed a great deal of skills and language. . . . A sampling of
her current skills includes her ability to expressively identify all the letters of
the alphabet presented in random sequence. She knows her shapes and colors,
she can count up to 12 items, and she has an extensive vocabulary (several hun-
Toward a Behavior of Reciprocity 143
dred words). Additionally, she has become proficient in categorizing items
among nine different groupings. I was recently quizzing her in the car and
asked “What’s a zebra?” “It’s a animal.” “What’s a triangle?” “It’s a shape.”
“What’s a couch?” “It’s furniture.” “Who’s William?” “It’s a person.” “What is
a w?” “It’s a letter.” “What’s a helicopter?” “It’s something you ride in.”
“What’s a bathing suit?” “It’s clothes.” “What’s cake?” “It’s food.” (p. 369)
As the mother wrote, “I present these examples to illustrate that many of the things
that Rebecca knows are quite advanced for a child her age. I am convinced that Re-
becca is a highly intelligent child. Her teachers tell me this constantly. In a way, that
makes her deficits all the more maddening” (p. 369). What are these deficits that are
so maddening to her mother? As the mother laments,
If, for example, I enter the kitchen after my morning walk and [my two daugh-
ters] are sitting at the kitchen table eating breakfast, Rebecca might glance up
at me for a second and then look away. I have to walk up to her, get in her face,
and force the interaction (“Hi Rebecca.” “Hi Mama.” “How are you?” “Okay.”
“I love you.” “I love you, too.”). I have always found the contrast between my
two children to be the most obvious and the most painful at mealtimes. Holly
is such a talkative and observant child, and Rebecca will be sitting there like a
sphinx, unable to participate in the give and take.
We find ourselves continually trying to draw her into our conversations.
“Rebecca, what are you doing?” “I’m eating.” “What are you eating?” “Pasta.”
“Good. What’s pasta?” “It’s a food.” “Good! Is it delicious?” “Yes.” “Say, ‘It’s
delicious.’ ” “It’s delicious.” (p. 368)
Furthermore, as the mother describes, “One big problem that we have recently
been tackling concerns Rebecca’s compliance during her [behavioral therapy] ses-
sions. At times Rebecca becomes very silly … We had decided to completely ignore
Rebecca’s behavior during these incidents and to revert to a simple command pre-
sented over and over until Rebecca would get bored and comply. Unfortunately, this
tactic did not succeed in extinguishing the noncompliance (it was going on for more
than a month), so we are now resorting to putting Rebecca in time out, which we have
determined is an aversive for her” (pp. 369–370). Such an approach might be helpful
for teaching a child to see the world through your eyes, which is the promise of
Bridges for Children with Autism (bridgesABAtapes.com), an internet company that
sells ABA therapy training tapes, but recall that Sarah, the girl on the eBay button—
and perhaps Rebecca, also—wished that others could see the world through her eyes.
How can we do that?
both typical and atypical development. For example, Herman (2002) wrote the follow-
ing in her essay titled, “What Parents Do to Encourage Communication and Lan-
guage” regarding typical development:
The process of getting to know their new child involves parents noticing what
interests them and how they react. Parents watch to see what their baby looks
at and will often talk about whatever it is that appears to interest their child. In
this way, the parent follows the baby’s lead. For example, if the baby gazes to-
wards the light, the parent may comment “are you looking at the light?” In this
way, the parent imposes meaning on the baby’s actions, even though the baby’s
actions at this early stage are without any specific purpose. Eventually, this
teaches the baby that actions lead to responses. In addition, the fact that com-
munication is closely tied into whatever activity the baby is engaged in helps
the baby begin to make sense of the stream of words they hear.
Herman wrote that toward the end of the first year of life,
An important behaviour to emerge at this time is the development of joint at-
tention. This is a natural development from the parent following the baby’s
lead and talking about the child’s focus of attention, as described above. Babies
begin to be more aware of when they and their parents are focusing on the same
object or activity. By the age of 9–12 months, they are able to follow their par-
ent’s line of vision and make use of pointing gestures. This helps them to begin
to match the language they hear with the focus of attention. Indeed, where par-
ents follow the infant’s focus of attention when providing language, infants’
vocabulary acquisition has been shown to proceed at a faster pace.
But what about the child who is delayed in developing the ability to follow his par-
ent’s line of vision? What about the child who is delayed in developing the ability to
make use of pointing gestures, that is, to follow a parent’s manual point or to make his
own pointing gesture? Or even to make his own reaching gesture? Experience sug-
gests that this is when parents—and professionals—need to enact even more reciproc-
ity, need to share even more of the child’s world, need to follow even more of the
child’s lead, and need to become something of a detective to discern the ways that the
child is expressing joint attention and social and emotional reciprocity.
Consider the detective work effectively accomplished by Robert Hughes, a
Chicago writer, who chronicled his life with his autistic son Walker in a critically ac-
claimed book, Running with Walker. In an essay titled “Autism and Empathy,” pub-
lished in Chicago Parent magazine, Hughes (2004) wrote the following about 17 year-
old Walker:
He can’t converse, play a game, sit still, tie his shoes. He does every mainline
autistic behavior in the book: waves his hands and stares at reflected light,
shouts certain words and phrases over and over, rewinds his audiotapes until
they break. . . . But there is one quality he has in such abundance that it seems
almost to define him: empathy. Bouncing on his therapy ball, his throne in our
dining room, he knows his family’s hidden feelings no matter how well we
mask them.
Toward a Behavior of Reciprocity 145
Unfortunately, when he was much younger, his mother and I did not always
catch on to this depth of feeling in him. Since he never nodded “yes” and “no,”
much less enunciated those words in any consistent way, even some of his es-
sential character traits tended to stay under our radar. They were only revealed
in dramatic blips that slowly enabled us to see him in a new way.
One such moment came when he was four years old. I had just come home
from three days in the hospital undergoing tests for chest pain. The tests
showed that I had experienced one of those Middle-aged Dad Hypochondria
Alerts: My heart was fine; I was nuts. When I walked in our front door (as far
as Walker knew, back from the dead) he took my hand and pulled me over to
the couch. He got out a copy of Pinocchio, one of those Disney books a child
reads along with an audiotape, and turned the pages until he got to the place
where he wanted me to read to him.
It was the passage about Pinocchio saving his father from the whale. I
stopped in the middle of a sentence and stared at him, amazed. It was my odd,
silent four-year-old’s articulate way of telling his father of his love and con-
cern. Since then, [my wife] and I have read his strange behavior in the light of
the boy revealed that day: The one who feels far more deeply than he lets on,
who signals his thoughts and feelings in unconventional, but still very telling
ways.
It is those “unconventional, but still very telling ways” that parents, researchers,
clinicians, and members of society must seek to identify. As autistic advocate, Jim Sin-
clair, has written in an essay titled “Don’t Mourn for Us” (Sinclair, 1993):
The ways we relate are different. Push for the things your expectations tell you
are normal, and you’ll find frustration, disappointment, resentment, maybe
even rage and hatred. Approach respectfully, without preconceptions, and with
openness to learning new things, and you’ll find a world you could never have
imagined. Yes, that takes more work than relating to a non-autistic person. But
it can be done—unless non-autistic people are far more limited than we [autis-
tic people] are in their capacity to relate. We spend our entire lives doing it.
at their mothers, the children engage in more exploratory and creative behavior with
the toys, and the children show considerably more positive affect (Dawson & Galpert,
1990). These effects are independent of the child’s developmental level.
In another laboratory experiment (Field, Field, Sanders, & Nadel, 2001), autistic
children displayed more socially reciprocal behaviors after repeated sessions in which
the experimenter imitated their behavior, in contrast to a control group of autistic chil-
dren with whom the experimenter played responsively but not imitatively. During a
second session in this experiment, autistic children who were imitated by the experi-
menter increased in looking, vocalizing, smiling and playing with the experimenter;
during a third session, autistic children who were imitated by the experimenter in-
creased in being close to the experimenter, sitting next to the experimenter, and touch-
ing the experimenter.
Can these reciprocal behaviors be packaged into a treatment program—a program
that trains parents and others to behave more reciprocally with their autistic children?
The answer is yes, and empirical evidence demonstrates the effectiveness of such pro-
grams. One study (Mahoney & Perales, 2003) used relationship focused intervention
to enhance the social emotional functioning of autistic children by implementing re-
sponsive teaching with the children’s parents. Some of the behaviors that the parents
were taught included the following: join the child’s perseverative play; read the child’s
behavior as an indicator of interest; follow the child’s lead; respond to the child’s be-
havioral state; match the child’s interactive pace; and expect the child to react accord-
ing to his or her temperament or behavioral style.
The participants were the mothers of 20 young children diagnosed as being on the
autism spectrum. The mothers received weekly one-hour intervention sessions for 8 to
14 months. Before and after the treatment, both the parents and the children were as-
sessed with a set of measures, but it is important to note that the treatment—the re-
sponsive teaching—was delivered only to the parents. Post-treatment, the mothers
were observed to have increased in their responsiveness and their affect, which was
the predicted outcome, and to have decreased in their achievement orientation and
their directiveness, which was also the predicted outcome (although the decreases in
achievement orientation and directiveness were not statistically significant). Post-
treatment, the children’s interactive behavior was observed to have increased an aver-
age of 50% in affect, persistence, interest, cooperation, initiation, and joint attention.
All improvements were statistically significant, and the largest gain was in joint atten-
tion, which improved 84%.
Post-treatment, the children’s socioemotional behavior was rated by their mothers
as being significantly less detached, more socially reactive, and better regulated,
according to the Temperament and Atypical Behavior Scale (Bagnato, Neisworth,
Salvia, & Hunt, 1999). In addition, as observed by the researchers using the Infant
Toddler Socioemotional Assessment, the children increased in their self-regulation and
social competence (Briggs-Gowan, Carter, Irwin, Wachtel, & Cicchetti, 2004; Carter,
Briggs-Gowan, Jones, & Little, 2003).
The gold standard in treatment outcome research is the randomized clinical trial
(i.e., an experiment in which there is both a treatment group and a control group, with
each participant being randomly assigned to one of the two groups). After decades of
Toward a Behavior of Reciprocity 147
claims such as “thirty years of research demonstrating the efficacy of applied behav-
ioral methods in reducing inappropriate behavior and in increasing communication,
learning, and appropriate social behavior” in autism (U.S. Surgeon General’s Office),
there exists only one randomized clinical trial assessing the efficacy of ABA interven-
tion for autism (Smith, Groen, & Wynn, 2000; see Gernsbacher, 2003, for a review).
Unfortunately, the one randomized clinical trial of ABA intervention for autism pro-
duced no significant improvements in social interaction or communication.2
Consider in contrast a randomized clinical trial evaluating the effectiveness of a
social communication intervention. Like the intervention delivered in Mahoney and
Perales (2003); however, this randomized clinical trial (Aldred, Green, & Adams,
2004) delivered intervention to only the parents of autistic children. The treatment
involved “educating parents and training them in adapted communication tailored to
their child’s individual competencies . . . promoting highly sensitive adult responses,
where actions made by the child are interpreted by the adult as having meaning and
being related to the child’s assumed intentions and desires, and replacing [the par-
ents’] controlling and intrusive responses with responses aimed at facilitating the
child’s active communication exchanges” (p. 1421–1422). Fourteen parents of autis-
tic children were randomly assigned to the treatment group, and the same number was
randomly assigned to the control group. The results of this randomized trial were quite
impressive.
Analysis of a 30-minute parent-child free play session by coders who were naïve
as to whether parents had been in the treatment or the control group identified several
statistically significant changes. First, parents in the treatment group increased 7.3% in
their synchronous communication, which comprises comments, statements, or ac-
knowledgements that maintain the child’s interaction; in contrast, parents in the con-
trol group decreased 7.6% in their synchronous communication. Second, parents in the
treatment group decreased 7.1% in their asynchronous communication, which com-
prised statements aimed at redirecting, controlling, or making demands on the child to
respond; in contrast, parents in the control group increased 7.6% in their asynchronous
communication. Third, parents in the treatment group increased 6.8% in their recipro-
cal communicative acts, which comprised verbal and non-verbal behaviors that share
communicative intent, while parents in the control group decreased 2.5%.
What effect did these parental changes have on their children? As measured by the
Autism Diagnostic Observation Schedule (Lord et al., 1989), children whose parents
received treatment were shown to increase significantly in their reciprocal social in-
teraction, their social engagement, their social rapport, their social responses, and their
spontaneous initiation of social interaction. The children also demonstrated dramatic
improvements in their language development, on the parentally reported MacArthur
Communication Development Inventory (Fenson et al., 1993). As shown in Figure 1,
children whose parents received treatment improved dramatically in their expressive
vocabulary, whereas children whose parents were in the control group did not. As
2. Although the original article reports significant effects on language development, there was an error in data
analysis, and an erratum was subsequently published (Smith, Groen, & Wynn, 2001).
148 MORTON ANN GERNSBACHER
Expressive Vocabulary
Vocabulary Size (on MCDI) 250
200
100
50 Control Group
0
Pre-Treatment Post-Treatment
Receptive Vocabulary
250
Vocabulary Size (on MCDI)
200
Treatment Group
150
50
0
Pre-Treatment Post-Treatment
shown in Figure 2, children whose parents were in the treatment group as well as the
control group improved in their receptive vocabulary.
Last year he got interested in the gods of Egypt; who knows why. And we don’t
know where this came from, this absolute intense interest in hairless dogs. We
don’t know why hairless dogs. But, my husband and I are cat people. We now
have a hairless dog.
In each of these alternate scenarios, the parents’ behaviors embodied an attitude of
reciprocity. As Greenspan and Weider (1998) have warned, “This can be hard. It’s nat-
ural to want to take over . . . You need to remind yourself to fight this tendency. Your
child will take the most pleasure in activities he chooses himself” (p. 140). Without
embodying an attitude of reciprocity and working toward a behavior of reciprocity, it
is unlikely that enjoyment will be defined by reciprocity, that is, “experienced or felt
by both sides” (American Heritage Dictionary of the English Language, 2000).
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Book Review
Barbara J. King
One hot summer day, infant Rosie was trying to get herself from an outdoor area,
where she was baking in the full sunshine, to an indoor room with air-conditioning. To
do this, she needed to lift up a flap covering a small door, but the flap was too heavy
for her to manage. Rosie began to make sounds of distress. Hearing these, Rosie’s
Dad, Joe, roused himself from the shade of a peach tree, walked over, and lifted the
flap for his daughter. As Rosie went indoors, Joe headed back to his patch of shade.
Why open a review of a book on parenting by highlighting an event of such a rou-
tine nature? Joe and Rosie are not humans; they are cotton-top tamarins, small mon-
keys that come from South America. And when Rosie was born, in captivity four
months before the door-flap incident, things hadn’t gone smoothly at all. Rosie’s
mother, Chartier, and dad Joe, rejected her and her sibling Ira (tamarins give birth to
twins).
When he helped Rosie escape the summer heat, then, Joe acted like a good Dad
not because he’s a tamarin and that’s what all tamarins do, or because his genes had
programmed him for paternal care. He did so because he had gained experience at
good parenting, through Harriet Smith’s self-devised, in-home monkey parenting pro-
gram. Joe had been hand-reared by Smith in the early 1970s, and thus had grown up
without benefit of knowing how tamarins are supposed to raise their young. When he
matured enough to mate and father offspring, Joe, together with his mate Chartier,
forcefully rejected several sets of twins, monkeys that then had to be handraised also
by Smith.
Parenting for Primates is Smith’s account of how tamarin-raising led her to under-
stand that nonhuman primates learn to be good parents from experience, and can over-
come even a rocky start as Joe did. Her account of how she broke the cycle of poor
parenting makes absorbing reading. Because Smith is not only a monkey-observer but
also a clinical psychologist, her main point is to show that what is true for Joe,
Chartier, Rosie, and Ira, can be true for a human family as well.
In addition to thinking across species about parenting, Smith thinks cross-culturally:
“Training for parenthood is by apprenticeship for both boys and girls in most pre-
industrial societies. . . . This process of experience first, parenting second, is reversed
in contemporary Western culture: we marry and establish our households first, and
153
154 BARBARA J. KING
then get our childcare training on the job. Both mothers and fathers may be in the same
boat, if neither have babysat younger siblings or other young children, and both may
question their abilities as parents when parenting doesn’t come ‘naturally.’”
Fathers may be particularly disadvantaged by this lack of experience: “Fathers,
whose role with infants has long been considered optional, may have little desire at
first to become involved. They step aside while their wives become competent moth-
ers by trial and error, with a little advice from family or experts thrown in.” Yet re-
search shows clearly that “[w]hen fathers start taking care of their babies, the babies’
responsiveness increases” (pp. 104–105).
Smith conveys many valuable lessons about the healthy emotional development of
human children in a family setting. The crux of her message is this: “Adequate par-
enting increases our chances of ensuring our own ‘immortality’: when our offspring
grow up and reproduce, they pass on our genes to future generations. And yet, the fas-
cinating and complex ways in which primate parenting behavior varies with charac-
teristics of the environment, the social context, and individual experience shows us
that parenting behavior is not totally determined by our genes. The flexibility and mal-
leability of primate parenting behavior reveal that we have the ability not only to
change our behavior but to make conscious choices about the kinds of parents we wish
to be” (p. 11).
This last sentence is one I could have borrowed for my editorial in this inaugural
issue of the Journal of Developmental Processes. Smith’s perspective on parenting
emerged from an unusual career trajectory. First earning a PhD in comparative prima-
tology, Smith carried out research on cottontop tamarins in the laboratory. For the next
30 years, she kept a colony of these monkeys at her home. (Smith makes a point of
saying that “monkeys, like other wild creatures, should not be kept as pets,” so the
book is a bit steeped in a do what I say, not what I do framework.) From that base,
Smith went on to earn a post-graduate degree in clinical psychology, establishing a
practice with, of course, human clients.
This blended background is both a strength and weakness of the book. Many
primate-related books focus on chimpanzees, bonobos, or gorillas—the African great
apes. This makes good sense given that these apes are humans’ closest living relatives,
yet it is refreshing to find a popular counterpart to the work done by researchers such
as Jeffrey French, Charles Snowdon, and John Terborgh in the world of tamarin and
marmoset academic research. Twin-birthing, family-living mini-monkeys are the per-
fect exemplars for Smith’s point about primate plasticity.
It’s a strength as well that Smith continues on from a discussion of primate infancy
to encompass juvenility and adolescence. It’s not all about the cute phase. Smith freely
offers opinions on contentious matters. One example: “That human adolescents are fas-
cinated with sex is a normal, healthy reflection of their primate heritage,” followed by
advice for how parents may enable their teenagers to resist temptation (p. 204). An-
other: “A family with more than one capable adult sharing the responsibility for chil-
dren, regardless of gender, has a better chance of positive outcome” (p. 298); of course,
she means the parents’ gender—not the children’s—in a welcome advocacy for loving
families of all kinds.
Book Review 155
Indeed, Smith zeroes in on societal patterns that affect parenting. Citing statistics
about dual-career couples and working mothers, she notes that in some cases daycare
is not a preference but a necessity, and laments the resources available: “Almost half
a million childcare workers (mostly women) are paid less than workers in 99 percent
of occupations in the United States today. The low pay offered to young females who
work in daycare centers in the United States sends the message that there is almost no
job less important than childcare” (p. 131). This matters, of course, because stable and
long-term relationships between babies and caregivers matter: “A baby’s best chance
for receiving quality care is having a babysitter that knows him, likes him, and wants
to please him. . . Quality daycare given by nonkin babysitters does not have to be a
contradiction in terms” (p. 132).
Yet I can’t give the book a pure rave. Comparative primatology is a good thing, but
can be pushed too far, as when Smith jumps effortlessly from human to New World
monkey behavioral patterns: “At the extremes of human fatherhood are titi-like fathers
(albeit very few) who are their children’s primary caretakers, and squirrel monkey-like
fathers, who play no role in their children’s development after conception” (p. 87). A
flat conflation of fathering in a species that is well-adapted and clever with fathering in
a species that creates linguistic-cultural norms made me quite uneasy.
Further, readers may sense that the book is dated. Smith reports quite a number of
older studies, still valuable, but there’s a somewhat stale flavor to some of the analy-
sis. Primatologists have described far too much variation in social organization within
species for terms like “harem” (for gorillas) or “solitary” (orangutans) to be relevant
any longer. It is simply incorrect to assert that no nonhuman primate females undergo
menopause. And to say that “twenty years ago, most of the thinking about primate be-
havior was based on studies of rhesus monkeys and other macaques” (p. 95) is strange,
given that ape fever had gripped primatology by the mid-1980s and much was flow-
ing to us from long-term studies of chimpanzees, gorillas, and orangutans, not to men-
tion baboons and other non-macaque monkeys. Suffice to know that although Smith
thanks various primatologists for reading chunks of the manuscript, an overall keen,
and scientific, editing eye was still needed.
More significantly, Smith does not always give the book’s topics the depth of cov-
erage they deserve. Some of most exciting work in parenting is not just about top-down
socialization, but about fully contingent and co-created behavior understood through a
dynamic-systems perspective. The notion of the family as a system, with a change in
one part affecting all, so that mutual transformation is possible, informs works rang-
ing from Murray Bowen’s seminal Family Therapy in Clinical Practice to Fivaz-
Depeursinge and Corboz-Warnery’s The Primary Triangle to Stanley Greenspan and
Stuart Shanker’s The First Idea—and indeed articles in this first issue of JDP.
As the examples I have chosen indicate, Smith veers toward a systems understand-
ing, in which each partner affects the other within a family, and in which the larger so-
ciety affects the family. I appreciated, for instance, her discussion of the concept of
micro-environment (p. 352), the idea that each child’s developmental trajectory is
affected by a constellation of factors in his or her environment (including the genetic
environment). What I missed was an appreciation that this isn’t just one partner or one
156 BARBARA J. KING
level of society affecting another in a certain environment, but two partners negotiat-
ing and co-creating behavior and meaning, and family and society mutually construct-
ing each other.
Still, Smith’s message is very much needed in a gene-besotted society. KNOW
YOUR DNA, blares a headline on Scientific American’s front cover (January 2006).
The subtitle is: Inexpensive gene readers will soon unlock the secrets in your personal
double helix. Harriet Smith’s thesis is that the most fascinating secrets of primate par-
enting lie not in DNA but the complex world of social plasticity and nurturing. When
Joe, the tamarin Dad, got up from the shade on a hot day, his exemplified this point to
his daughter Rosie; through Smith, we all benefit from his message.
Journal of Developmental Processes
Submission Guidelines
Description
The goal of the Journal of Developmental Processes is to provide a vehicle for
research and clinical studies that advance knowledge of the complexity inherent in all
developmental processes. The JDP encourages exchange of ideas across fields including,
but not limited to, animal behavior, anthropology, biology, education, linguistics, neuro-
science, occupational and speech and language therapy, primatology, psychiatry, psychol-
ogy, public policy, sociology, and social work.
The Journal is interested in both experimental and descriptive studies, including
basic research, detailed case reports, ethnographic analysis, and theoretical explorations.
Particularly welcome are innovative conceptual frameworks and methods that capture the
complexity of developmental processes as well as assessment procedures and interven-
tions that enable children and families to overcome mental health, developmental, social,
and learning challenges.
Submissions
Send queries and submissions on clinical aspects and applications to Asso-
ciate Editor Ira Glovinsky at ira1834@sbcglobal.net; all other queries and submissions,
and books for potential review, should go to Editor Barbara J. King at bjking@wm.edu
or Department of Anthropology, College of William and Mary, Williamsburg, VA, USA,
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style, e.g.,
please visit www.icdl.com
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