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Psychological Bulletin Copyright 1989 by the American Psychological Association, Inc.

1989, Vol. 105, No. 2, 179-197 0033-2909/89/$00.75

Sensitive Periods in Development:


Structural Characteristics and Causal Interpretations
Marc H. Bornstein
National Institute of Child Health and Human Development
and New \brk University

The presence or absence of a particular experience at a particular time in the life cycle may exert an
extraordinary and dramatic influence over structure or function well beyond that point in develop-
ment. Such sensitive periods are thought to be widespread in animal and in human neurobiology
and psychology. A comprehensive treatment of the sensitive period needs minimally to include infor-
mation about its structural characteristics as well as an interpretation of its causes, including why
the sensitive period arises in terms of the natural history of the species and how the sensitive period
is regulated in terms of physical, physiological, and psychological processes. This article provides a
framework for research and theory concerning specific sensitive periods and the sensitive period
generally conceived. The framework delimits four sets of parameters, which encompass 14 structural
characteristics that define sensitive periods, and two levels of causal interpretation that guide re-
search and theory into sensitive periods however they may be manifested.

Mary had a little lamb Sensitive periods are meaningful in psychology, and particu-
Its fleece was white as snow,
larly in developmental psychology, for several reasons. First,
And everywhere that Mary went
The lamb was sure to go. sensitive periods give concrete evidence of the continuing con-
trol that experience may exert on development and on the na-
Scientists who study structure or function from all but an ture of mature structure and function. Relatedly, the influence
entirely static perspective inevitably confront the truism that of experience displaced over time testifies to the force of coding
dynamic animate phenomena are shaped by endogenous and and retention of information in memory. Second, the fact that
exogenous forces interacting through time. Those forces do not sensitivity to experience waxes and wanes through the life span
exercise equal effects at all times, however; indeed, it is now illustrates clearly the interactional character of development.
common to speak of unique phases in the ontogeny of many Third, manifestations of sensitive periods in development sup-
different structures and functions when evolving transactions ply convincing testimony to the existence of discrete phases in
among life forces profoundly influence development. These the life course. Last, that specifiable early experiences may have
phases are unique in that during select times in the life cycle far-reaching consequences in ontogeny renders the sensitive pe-
many structures and functions become especially susceptible to riod of potentially great practical significance. For these rea-
specific experiences (or to the absence of those experiences) in sons, presumably, sensitive periods have been the subject of
a way that alters some future instantiation of that (or a related) popular appeal, theoretical fascination, and empirical scrutiny
structure or function. So, during such sensitive periods in devel- since their earliest discovery.
opment specific experiences may exert a marked influence over Sensitive periods were first identified in ethology and in ex-
future history. perimental embryology: Chicks hatched in the absence of a hen
were observed to follow any moving object to which they were
exposed in the first days after hatching, but not later (Spalding,
1873). Certain cell masses were found to be affected by intrud-
This research was supported by Research Grants HD20559 and
HD20807 and a Research Career Development Award (HD00521) from
ing chemicals during a particular stage in their ontogeny but
the National Institute of Child Health and Human Development and not earlier or later, and certain cells transplanted at a particular
Research Grant BNS 84-20017 from the National Science Foundation. time in their ontogeny were found to assume the characteristics
Preparation of this article was partially supported by a grant from the of host location cells and thrive, but to wither if transplanted at
Center of Developmental Education and Research, Tokyo, and was times preceding or following (Spemann, 1938; Stockard, 1907,
completed during my tenure as Visiting Professor, first at the Faculty of 1921). Not long after these initial reports, sensitive periods
Education of the University of Tokyo and later at the Laboratoire de came to be implicated in a plethora of fields germane to psycho-
Psychologic du Developpement et de 1'Education de 1'Enfant of the Sor- logical inquiry: At different times, sensitive periods have been
bonne. I thank H. Bornstein for comments.
seen as relevant to studies of brain and bodily structure and
Correspondence concerning this article should be addressed to Marc
H. Bornstein, Child and Family Research, National Institute of Child function across the phylogenetic series as well as in studies of
Health and Human Development, Building 31, Room B2B15, 9000 survival, social, and mental competence in infrahuman animals
Rockville Pike, Bethesda, Maryland 20892. and in human beings.

179
180 MARC H. BORNSTEIN

Given so broad a sweep of theoretical interest and scope of The fact remains that the sensitive period reflects a develop-
experimental investigation, it would be natural to expect a cer- mental event of impressive conceptual unity and coherence
tain heterogeneity of focus and perhaps of definition about sen- even across the diversity of biological, psychological, and socio-
sitive periods. In fact, the typical investigative style adopted by logical disciplines in which it has been studied. The sensitive
researchers of sensitive periods historically has been to center period possesses a common set of characteristics that define its
attention on the intersection of a particular phenomenon with structure and invokes a common set of interpretations that per-
a particular species: sensorimotor connectivity in aplysia (e.g., tain to its cause. The central goal of this review is, therefore,
Montarolo, Goelet, Castellucci, Morgan, Kandel, & Schacher, to construct a framework that makes explicit those structural
1986), cocoon preference in ants (e.g., Jaisson & Fresneau, characteristics and causal interpretations essential to under-
1978), aggression in mice (e.g., Cairns, Hood, & Midlam, standing the deeper nature of this significant and ubiquitous
1985), imprinting in ducks (e.g., Hess, 1973), cortical cell speci- developmental event. Comprehensive characterization is vital,
ficity in cats (e.g., Hubel & Wiesel, 1970), sociability in dogs if not imperative, to meaningful analysis, and a proper descrip-
(e.g., Scott, 1962), emotionality in monkeys (e.g., Harlow & tive framework promises significant implications for both re-
Harlow, 1969), or language acquisition in human beings (e.g., search on and theory about the sensitive period. The ultimate
Lenneberg, 1967). This orientation resulted inevitably in a re- intentions of this review are, therefore, to guide future investi-
markably diverse and disparate, if not daunting, experimental gations of individual sensitive periods and by doing so to illumi-
literature, as noted by several previous reviewers (e.g., Bateson, nate their nature as well as that of the sensitive period per se.
1979; Bornstein, 1987; Colombo, 1982; Immelmann & Suomi,
1981; Oyama, 1979; Scott, 1978). However, two central (and A Sensitive Period Framework:
consensual) conclusions of individual investigations and of col- I. Structural Characteristics
lective reviews alike are, first, that sensitive periods reflect idio-
syncratic and multifaceted biological, psychological, and socio- The first question that arises in identifying a sensitive period
logical phenomena and, second, that the sensitive period is not is descriptive, that is, what are its particular structural charac-
a monistic concept. teristics. (I use the phase structural characteristics to stand for
Investigation into a sensitive period seems normally to tra- the list of descriptive parameters of sensitive periods.) This is as
verse two stages. Initially, the sensitive period undergoes de- it should be: The empirical characterization of parameters of
scriptive treatment, followed by experimentation organized to the sensitive period is a first-order prerequisite to comprehen-
quantify its several parameters. The full details of individual sive and systematic analysis of its function or meaning. A sec-
sensitive periods are never unabridged however, since empirical ond prerequisite, taken up later, is investigation about cause.
examination tends usually to focus on single parameters. More- In one notable theoretical overview, Nash (1978) considered
over, the concept of the sensitive period per se has failed to reach four parameters of sensitive period structure, including onset,
a high level of theoretical development. Specifically, individual terminus, and intrinsic and extrinsic factors that specify, re-
investigators of sensitive periods have been reluctant to ac- spectively, the triggering maturational event in the organism
knowledge an underlying unified framework from which to ap- and the influential experiential event outside the organism. On
proach the sensitive period. This conceptual shortfall is, it the earlier suggestion of Moltz (1973), Colombo (1982) added
would seem, the unhappy by-product of two conditions. First, a fifth characteristic to Nash's four, the organismic system that
the sensitive period has two distinct construals: In one, norma- is affected by experience during the sensitive period. In actual-
tive experience in the sensitive period is necessary for or advan- ity, however, the sensitive period is comprehensively described
tageous to normal development, and in the other, noxious expe- by at least 14 distinguishing, essential, and operationally defin-
rience in the sensitive period may harm the organism. These able structural characteristics. These 14 structural characteris-
separate interpretations are infrequently mixed in discussions tics may be categorized into four distinctive sets. The first set
of the sensitive period, and so tend to obscure a unified view. describes temporal and intensive contours of the sensitive pe-
The second rationale supporting a pluralistic view of sensitive riod when it occurs in the life cycle, and links five structural
periods is that, as stated earlier, descriptions of sensitive peri- characteristics: (a) developmental dating, (b) onset, (c) offset,
ods, however detailed, and experiments on sensitive periods, (d) duration, and (e) asymptote. The second set unveils the
however defining, have tended to concentrate on the individual- mechanisms involved in sensitive-period change, and incorpo-
ity of particular sensitive periods. In addition to the overrich rates three characteristics: (f) experience, (g) system, and (h)
variety of individual types and the multiplicity of facets in any pathway. The third set examines consequences of the sensitive
one type, reports of sensitive periods appear in widely distrib- period, and unites four characteristics: (i) outcome, (j) manner,
uted and nonoverlapping literatures. Working in highly circum- (k) outcome conditions, and (1) duration. The fourth set takes
scribed areas and confronting the near bewildering complexity into account evolutionary and ontogenetic time scales with re-
of individual sensitive periods, researchers seem therefore to spect to sensitive periods, and involves two characteristics: (m)
have actively eschewed (indeed, many have lobbied against) gen- variability and (n) modifiability.
eralization. These main factors have tended to impede develop-
ment of a perspective of the sensitive period as unified, with Structural Characteristics of the Sensitive Period
the inevitable result that the overarching issues of the structural
character and causal interpretation of sensitive periods in gen- In this section, I define and illustrate each of the 14 promi-
eral have been insufficiently addressed. nent structural characteristics of sensitive periods. This taxon-
SENSITIVE PERIODS IN DEVELOPMENT 181

omy represents one way of organizing theory and research in of the local environment or attaching socially to a source of
sensitive periods. In selecting examples to represent particular nurturance, ought logically and naturally to be fixed to infancy
sensitive periods, I have attempted to invest this scheme with a and ought also to transpire only once in the life span. In implicit
current of continuity by referring when possible to the two most support of this belief, some sensitive periods are correlated with
popular subjects of sensitive-period study, namely visual sensi- specific developments that take place in early life and only once,
tivity and imprinting. However, perception and social attach- as at organogenesis, at first eye-opening, or at the onset of loco-
ment are not the subjects of this review; no one kind of sensitive motion.
period is. In addition, I have elected in some cases to reference It is also the case, however, that sensitive periods in infancy
special or idiosyncratic examples of sensitive periods because have simply been investigated most often. Exceptions show that
they constitute particularly apt or telling instances and to draw sensitive periods can also arise late in development: The sensi-
upon contrasting or complementary examples in order to throw tive period for sexual imprinting in maturing zebra finches
a particular issue into relief. The text also provides some nu- demonstrates that sensitive periods are not limited to the new-
merical values; it must be understood, however, that quantita- born period (Bateson, 1979), as does the sensitive period for
tive estimates of sensitive-period parameters are commonly ac- maternal responsiveness to young of the species in goats (Gub-
knowledged to fluctuate with species, ontogeny, methodology, ernick, 1981; Klopfer, Adams, & Klopfer, 1964), in dairy cattle
and other factors.' Finally, not all features of all structural char- (Hudson & Mullord, 1977), and in sheep (Poindron, Levy, &
acteristics in all systems have been studied; indeed, not all struc- Krehbiel, 1988; Poindron, Martin, & Hooley, 1979). Although
tural characteristics of any one system have been exhaustively sensitive periods are thought normally to occur only once in
researched. This review is perforce illustrative. the life-cycle, some sensitive-period alterations in structure and
For purposes of this discussion, consider a system to specify function can be expected to take place more often. Indeed, this
the structure or function that is the main subject of sensitive- would be expected for sensitive periods for maternal responsive-
period analysis. What dimensions underlie sensitive-period ref- ness in multiparous goats, cattle, and sheep for identification of
ormation? individual young. Apparently, then, some sensitive periods may
occur at sundry points in the life cycle and may recur numbers
Temporal and Intensive Contours of times.
How is developmental dating of the sensitive period better
Five characteristics demarcate the profile of the sensitive pe- calculated, quantitatively or qualitatively? In terms of real time,
riod when it occurs. They concern timing and change associated in terms of developmental time in the life cycle of the system, or
with sensitive periods. in terms of a specifiable developmental event? Is developmental
timing of the sensitive period better specified in terms of con-
Developmental Dating ceptional age or in terms of postnatal age?
In practice, most investigators use postnatal age in dating
When in the life cycle of the system the sensitive period occurs, sensitive periods: Contact comfort needs to be available be-
its frequency, and quantification of its temporal component. De- tween the period of birth and 250 days to ensure normal social
velopmental dating of sensitive periods is requisite to first-order behavior in the rhesus monkey (Harlow & Harlow, 1969); nor-
characterizations. Between eye-opening and about 3 months mal song must be heard in the period between 10 and 50 days
later, the kitten visual system is uniquely susceptible to visual for normal song to develop in the song bird (Marler, 1970); fa-
experience, yet outside this period environmental exposure has miliarization with humans must obtain in the period between
nowhere near the equivalent effect (Sillito, 1983). In maturity, 18 and 63-91 days for socialization in dogs (Freedman, King,
male zebra finches raised early in life by Bengalese finches al- & Elliot, 1961); primary socialization must be incurred in the
most exclusively court Bengalese finches, even if they are in period between 20 and 45 days to eventuate in domestication in
later life exposed extensively to conspecific females (Immel- the silver fox (Belyaev, Plyusnina, & Trut, 1985); social isolation
mann, 1972). Two principal questions arise with respect to de- must be instituted in the period between 25 and 45 days for a
velopmental dating: first, When in the life course of a system heightened level of object contact in rats (Einon & Morgan,
does the sensitive period occur? and, second, How often does 1977); shelter must be secured in the period between 30 and 60
the sensitive period repeat? A third question is how dating of days to maintain reactivity to stimulation in the gerbil (Clark &
the sensitive period is most meaningfully calculated. Galef, 1979); and exposure to the visual environment must fol-
Most investigators believe that sensitive periods are standard, low in the period between 30 and 90 days for modification of
if not circumscribed, to early development, and many suppose the functional organization of the visual cortex in the cat (Sil-
that they are once-in-a-lifetime events (e.g., Bateson, 1979; lito, 1983).
Boothe, Vassdal, & Schneck, 1986; Brook, 1972; Caldwell, Of course, some cases mandate dating by conceptional age,
1962; Colombo, 1982;Pettigrew, 1978). Much sensitive-period
theory and research are predicated on these opinions. Following 1
For example, methodological regimen influences quantitative val-
Child (1921), Scott (e.g., 1986) proposed the general principle ues: Presson and Gordon (1979) report that on one methodology Blake-
that systems would be most sensitive to modification of their more and Van Sluyters placed the end of the sensitive period for binocu-
developmental trajectory during periods of their most rapid larity in the kitten at about 8-10 weeks, that on a second Hubel and
(re)organization, as in growth. Moreover, many sensitive-period Wiesel placed it at about 12 weeks, and that on a third Timney placed
alterations, such as adapting perceptually to the physical nature it at about 16 weeks.
182 MARC H. BORNSTEIN

as when prenatal experience is critical. Hill and Przekop (1988) in real time, and most agree that the onsets of sensitive periods
found that if mother rats are put on a low-sodium diet on or tend to be quite rapid. For example, the onset of the sensitive
before 8 days postconception, their pups fail to develop taste period for suceptibility to noise-induced cochlear damage in
sensitivity to sodium, but mothers who begin a low-sodium diet the mouse lasts 5 days, or less than 1% of the mouse's 527-day
10 or more days after conception give birth to normal pups. actuarial life span (Henry, 1983). Likewise, the onset of the sen-
Brook (1972) provided evidence that the sensitive period for sitive period for binocularity has been reported to begin "sud-
adipose-cell replication in humans to hormonal and nutritional denly" in the cat, coincidental with eye-opening (Hubel & Wie-
circumstances extends from approximately 30 weeks gestation sel, 1970, p. 434); the kitten's rise in sensitivity has been submit-
to the age of about 1 year. ted to parametric scrutiny and found to dawn between Day 9
When choice exists in dating, controversy appears. Opinions and Day 13 (Freeman, 1978).
differ, for example, with respect to computing the time of the Systems do not always or necessarily reach full susceptibility
sensitive period in imprinting in ducklings. Hess (1959) calcu- immediately at onset, however. For example, kittens who expe-
lated the sensitive period for imprinting in terms of age in real rience monocular deprivation at the start of the sensitive period
time after hatching, whereas Gottlieb (1961) later calculated the may lose binocularity, but apparently loss related to deprivation
same sensitive period in terms of age in real time after concep- at that time is only transient, because binocular experience in
tion, claiming that such a representation reduces variation in the balance of the sensitive period can lead to a significant de-
temporal parameters of the sensitive period. Landsberg (1975) gree of recovery (Olson & Freeman, 1978).
showed that the two age-dating systems contributed informa- In contrast with prevailing opinion about sensitive-period on-
tion valuable to understanding the ontogenetic nature of the sets, many researchers theorize that offsets of sensitive periods
sensitive period: developmental age for endogenous influences are typically gradual (e.g., Hinde, 1962). For example, the onset
and posthatch age for experience-related effects. of the sensitive period for human binocular vision is believed to
Some researchers have dated sensitive periods in terms of ac- endure over a period of about 1 month, whereas the offset is
tual life-span events instead of age. For example, undernutrition believed to taper over about 5 years (Banks, Aslin, & Letson,
must be endured for the period of suckling to have lasting effects 1975). Likewise, onset of the sensitive period for filial imprint-
on social behavior in rats (Byrne & Smart, 1980); exposure to ing in the zebra finch is confined to a brief point in early life,
nonmimetic eggs must fall during the period of egg laying for whereas its offset is reported to linger into adolescence (Immel-
rejection in orioles (Rothstein, 1978); separation from the lamb mann&Suomi, 1981).
immediately after parturition engenders rejection by maternal Several exceptions limit strict generalization, however. Hill
ewes (Collias, 1956); and dogs' learning of territorial bound- and Przekop (1988) found the transition from maximal envi-
aries coincides with the advent of sexual maturity (Tinbergen, ronmental susceptibility to no susceptibility for the fetal rat
1951). A vulnerable period in human brain development has gustatory system to last only 2 days. Beatty, Dodge, Traylor, and
been postulated to coincide with the maturational spurt of ax- Meany (1981) delimited the temporal period when exposure to
ons and dendrites, glial multiplication, and myelination (Dob- testicular hormones affects development of rough play in male
bing & Sands, 1973). In the same vein, Almli and Finger (1987) rats; castration on Days 1 or 6 reduced male play, but castration
argued that dating by neurodevelopmental landmarks (e.g., my- on Days 10 or 20 did not, thus circumscribing the offset of the
elination) orders the literature on sensitive periods for behav- sensitive period for demasculinizing effects of testicular andro-
ioral recovery from neural insult, which is especially useful in gens to a maximum of 4 days' time. Buisseret, Gary-Bobo, and
cross-species comparisons. Imbert (1982) assessed the offset of the sensitive period for ori-
In point of fact, however, both quantitative and qualitative entation selectivity in kitten and found it to end abruptly in
dating systems share the same developmental events—concep- the rather narrow window of postnatal weeks 10-12. Similarly,
tion or birth—as reference points, only one uses chronological Elberger (1984) investigated the role of the corpus callosum in
time as a kind of postevent marker. It may be that researchers visual development in kittens and found that animals whose
resort to chronological specification when, for some reason, posterior corpus callosum was sectioned in Week 3 showed
other critical developmental events cannot be specified. deficits in visual acuity whereas those sectioned in Week 4 (or
after) did not.
Onset and Offset
The rise and decay of sensitivity in terms of setting event and Duration
time. What events govern the start and finish of the sensitive
period, when and how do they come into play, and how are they The temporal window of susceptibility. By definition the sen-
described? Are onset and offset better characterized quantita- sitive period endures within the confines of its onset and offset,
tively or qualitatively? Are they better characterized in terms of and its duration is among the most frequently described struc-
real time, in terms of developmental time as a proportion of the tural characteristics. How long does the system remain sensi-
life-cycle of the system, or in terms of a specifiable developmen- tive?
tal event? Are the growth and decay slopes of sensitivity to and The window of vulnerability is often an identifying character-
from the peak step functions or are they graded, and are they istic of sensitive periods, even when little if anything else is
linear? known about them. Thus, for example, sudden infant death
Researchers usually specify the onset of the sensitive period syndrome shows a strong, time-locked course on the basis of
SENSITIVE PERIODS IN DEVELOPMENT 183

which it has frequently drawn the attribution of a human sensi- Further, sensitive-period peaks are often presumed to center
tive period (e.g., Hunt & Brouillette, 1987). temporally with respect to duration, and to be unimodal. How-
Most investigators specify the temporal duration of the sensi- ever, Brook (1972) suggests that the peak of adipose-organ sen-
tive period in terms of real time. Examples abound and show a sitivity to nutrition effects in man is skewed to the onset of the
wide variation in the window of susceptibility; some prominent sensitive period. Counter-examples may also be found to the
ones corresponding to the examples of developmental timing assumption that sensitive-period peaks are unimodal. Henry
cited above (but recast by amount of time) are the following: A and Bowman (1970) acoustically primed mice from two pure
ewe must label her lamb in a period of less than .03-.08 days (45 strains (C57BL/6J and DBA/2J) and found a sensitive period
minutes-2 hours) after parturition to ensure acceptance (Col- between 12 and 26 days during which priming induced suscep-
lias, 1956; Pissonnier, Thiery, Fabre-Nys, Poindron, & Keverne, tibility to audiogenic convulsions in one strain and enhanced
1985); protein and messenger RNA (mRNA) must be synthe- susceptibility in the other. They also found that Fl hybrids
sized in a period of .04-. 12 days (1-3 hours) for long-term facili- manifested a bimodal sensitive period in which either parental
tation of sensorimotor connection in aplysia (Montarolo et al., strain would appear dominant depending on the age at which
1986); social isolation must be instituted in a period of 20 days hybrids were acoustically primed. Schutz (cited in Scott, 1962)
for a heightened level of object contact in rats (Einon & Mor- earlier reported a bimodal sensitive period for social attach-
gan, 1977); primary socialization must be incurred in a period ment in ducks: one peak for attachment to particular individu-
of 25 days to eventuate in domestication in silver foxes (Belyaev als formed early in the sensitive period, and a second peak for
et al., 1985); shelter must be secured in a period of 30 days to attachment to the species formed late in the sensitive period.
maintain reactivity to stimulation in gerbils (Clark & Galef, Basic to identifying and describing a sensitive period is delim-
1979); species-normal song must be heard in a period of 40 days itation of structural characteristics associated with its ontoge-
for normal song to develop in song birds (Marler, 1970); famil- netic timing. They include developmental dating, onset and
iarization with humans must obtain in a period of 46 to 74 days offset, duration, and asymptote. These parameters of a sensitive
to socialize dogs (Freedman et al., 1961); exposure to the visual period are relatively straightforward and empirically definable.
environment must follow in a period of 60 days for modification Nevertheless, many serious questions envelop parameters asso-
of the functional organization of the visual cortex in cats (Sil- ciated with ontogenetic timing of sensitive periods. For exam-
lito, 1983); and contact comfort needs to be available in a pe- ple, rates of change in sensitivity of a system during the tempo-
riod of 250 days to ensure normal social behavior in rhesus ral periods of the onset and offset are rarely studied; they may
monkeys (Harlow & Harlow, 1969). be linear (as is often presumed), or they may not. Mechanisms
Some researchers, although few in number, specify duration that trigger onset and offset are infrequently documented. Like-
in terms of developmental events. For example, undernutrition wise, questions concerning the ontogeny, temporal characteri-
must be endured for the period of suckling to have lasting effects sitics, and plasticity of the duration of a sensitive period often go
on social behavior in rats (Byrne & Smart, 1980), and exposure unraised, as well as unaddressed. The asymptote in the sensitive
to nonmimetic eggs must fall around the onset of laying to pro- period is a most intriguing yet underresearched structural char-
voke rejection in orioles (Rothstein, 1978). acteristic: By definition, sensitivity is always raised in the sensi-
tive period, but can sensitivity sometimes be lowered to protect
the organism from the environment? Would diminished sensi-
Asymptote
tivity still characterize a "sensitive period"? Clearly, specific
The nature and degree of change in sensitivity and the unifor- sensitive periods will be better understood, as will the concept
mity of sensitivity during the sensitive period. Is the sensitivity of the sensitive period more generally, when considerations of
threshold always altered to the advantage of the organism dur- ontogenetic timing are treated comprehensively.
ing the sensitive period? By how much is sensitivity reset during
the sensitive period? Is sensitivity level during the sensitive pe- Mechanisms of Change
riod better described as a plateau or as a peak? If a peak, where
in the temporal window does the peak occur? Is sensitivity a Three characteristics define structures wherein the sensitive
constant, or does it fluctuate during the sensitive period? period is shaped: the parameters of the outer and inner worlds
Actually, asymptotes of sensitive periods are not normally de- of the organism that are most immediately involved in the sen-
scribed. Most investigators seem to presume that sensitivity sitive period and the linkage between them.
level during the sensitive period holds constant, as for example
sensitivity to cochlear damage in mice (Henry, 1983). However, Experience
some researchers report that sensitivity is peaked, as for exam-
ple for cortical susceptibility in kittens (e.g., Blakemore & The effective stimulus event (or nonevent) in the sensitive pe-
Mitchell, 1973), for filial imprinting in mallard ducks (e.g., riod, its specific nature, its physical characteristics, and its ori-
Hess, 1959), for emotional behavior in dogs (e.g., Scott, Stewart, gins. Many investigators endeavor to provide reasonably pre-
& DeGhett, 1974), for domestication in foxes (e.g., Belyaev et cise data about effective stimulation for a sensitive period.
al., 1985), for social behavior in monkeys (e.g., Harlow & Har- Three questions arise immediately in considering the nature of
low, 1969), and for adipose-cell replication in human beings the sensitive period's special experience; they include, first, the
(e.g., Brook, 1972), although precise definitions for "peaked" specificity of experience, second, dimensions and features of the
temporal sensitivities may be lacking. experience, and, third, sources of the experience.
184 MARC H. BORNSTEIN

In his classic studies of the sensitive period, Stockard (1921) tonic function of the number of 30-min exposures the chicks
found that many different inorganic chemicals would induce had experienced. Suomi and Harlow (1975) found that 2-hr pe-
monstrosities in fish embryos as long as they were applied at a riods of peer interaction just 5 days a week could mitigate atypi-
specific time in ontogenesis. His results called into question the cal social behaviors of surrogate-reared monkeys.
specificity of the stimulus experience per se in the sensitive pe- A second set of parameters specifying physical dimensions of
riod. Time has shown that specificity of experience itself has a the experience concerns stimulus intensity. How intense must
great range. Some sensitive periods admit a spectrum of experi- the stimulus experience grow to be effective? During the sensi-
ence: During the sensitive period for cortical binocularity in tive period for raising avoidance-learning scores of adult rats,
kittens, visual axis misalignment or monocular deprivation will Denenberg (1968) found that lower levels of shock (0.2 mA)
be equally effective in influencing cell function (Levitt & Van were ineffective, whereas higher levels (0.5 mA) were effective.
Sluyters, 1982); during the sensitive period for imprinting, gulls A natural conclusion might be that stimulation and effect are
will form a social attachment to another gull or to a cage in linearly related, but they need not necessarily be. For example,
which they are housed (Evans, 1970); and, during the sensitive stimulus intensity could relate to effect in an inverted-U man-
period for maternal attachment, a ewe that licks any recently ner, as Denenberg suggests; in such cases, there may be "optimal
born lamb, not exclusively her own, will on this basis later dis- levels" of stimulation associated with sensitive-period experi-
tinguish that lamb from others (Poindron et al., 1988; Smith, ences. Other patterns of relations are also imaginable.
Van-Toller, & Boyes, 1966). Other sensitive-period experiences A third set of parameters specifying physical dimensions of
tend toward greater specificity: Gottlieb and Klopfer (1962) the experience concerns the sensory nature of the effective stim-
pointed out that ducklings imprint earlier on auditory stimuli ulus. For example, Gottlieb and Klopfer (1962) found different
than on visual ones; during the sensitive period for song learn- sensitive periods for visual versus for auditory stimuli in duck-
ing, white-crowned sparrows acquire the song of their own spe- ling imprinting.
cies, but will not acquire the song of other species (Marler, What are the principal sources of experience? In some cases
1970); and, during the sensitive period for egg recognition, ori- answers are clear, whereas in others answers are more ambigu-
oles reject brown-headed cowbird eggs from their nest, but do ous. Gottlieb (1983) found that during a sensitive period in per-
not reject eggs that differ from their own only in size (Rothstein, ception duck embryos must produce their own contact-con-
1978). Still other experiences are mixed in terms of specificity: tentment call in order to ensure a normal preference for their
During the sensitive period for orientation selectivity in kittens, species maternal call after hatching. Reppert (1985) contended
exposure to verticals or to horizontals maintains exclusively that the developing circadian clock is initiated in the suprachi-
vertical or horizontal sensitivity, respectively, but exposure to asmatic nuclei of the anterior hypothalamus by the maternal
diagonals maintains sensitivity to diagonal, vertical, and hori- host during a brief sensitive period in utero and is so main-
zontal (Leventhal & Hirsch, 1975). During the sensitive period tained until the opportunity for direct (external) photic entrain-
for imprinting in the duck, experience proceeds with the great- ment. The distinction between initiation and maintenance of
est facility with conspecifics, next best with similar species, and the sensitive period with regard to source is a provocative one,
least well with objects (Immelmann, 1972). and arises again in the interesting and complex case of the sensi-
Specifying physical dimensions of the experience rewards in- tive period for maternal bonding in ungulates (Poindron et al.,
vestigators invested in closely depicting the nature of a sensitive 1988). This sensitive period appears to be induced in the
period. A first set of parameters concerns stimulus duration. mother by the rise in estradiol associated with the term of preg-
How long must the stimulus be present (or absent)? (This ques- nancy and is augmented by genital (vaginal-cervical) stimula-
tion is intimately tied to that of duration of the sensitive period tion accompanying labor and expulsion; it is then sustained by
discussed above.) During the critical period for orientation se- exteroceptive cues in the offspring, including amniotic fluid, as
lectivity (between 3 and 14 weeks), kittens express greatest sen- well as by physical contact between mother and young through
sitivity around 28 days, and at this time as little as 1 hr of selec- licking and interaction (Keverne, Levy, Poindron, & Lindsay,
tive experience will completely transform the distribution of 1983; Pissonnier et al., 1985; Poindron et al., 1988). Thus,
orientation-sensitive cells in the cortex (less time was not re- sources of this sensitive period are in the mother, in the new-
ported); 2 or 32 hr additional experience will not exert a sig- born, and in interaction between the two.
nificantly greater effect than 1 hr(Blakemore& Mitchell, 1973).
During the critical period for imprinting in the mallard, as little System
as 4 min 49 s of exposure will lead to a preference lasting over
103 days (Schutz, 1972, cited in Immelmann & Suomi, 1981). The structure or function altered in the sensitive period. The
Additional questions are, Must the experience be present con- assumption that "something is changed" during the sensitive
tinuously, or may it be interrupted? Must it cumulate? For what period constitutes a central tenet of sensitive-period investiga-
proportion of the duration of sensitivity is experience effective? tion and theorizing, but the task of pinpointing the system that
Pettigrew, Olson, and Barlow (1973) found that very short-term is actually affected and defining its nature seriously challenges
repeated stimulation of neurons in kitten cortex induced most investigators. Three questions that are regularly posed
changes that mimicked permanent modifications typical of sen- concerning the nature of that system include, first, the observ-
sitive periods, but these changes were less pronounced and en- able or nonobservable character of the system, second, its uni-
dured only transiently. Zajonc, Reimer, and Hausser (1973) tary or pluralistic configuration, and, third, the level at which
found that object attraction in 1-day-old chicks was a mono- the affected system functions.
SENSITIVE PERIODS IN DEVELOPMENT 185

Is the system directly observable and measurable, or must the phenomena in rodent social play (Beatty et al., 1981), and that
system be inferred from change that is observed and measured plasma corticosterone serves as a pathway of sensitive-period
later? Most investigations of sensitive periods proceed on a phenomena in filial imprinting (Landsberg & Weiss, 1976).
"first manipulate developmental timing and experience and Hirsch and Tieman (1987) argued that endogenous neurotrans-
later assess outcome" modus operandi; in this scheme, evalua- mitters help to determine whether activity-dependent changes
tion of the affected system itself may or may not take place. eventuate in synaptic organization during sensitive periods in
Some investigators actually measure intervening systems kittens. Indeed, Lauder and Krebs (1986) have pointed out that
affected. Rothblat and Schwartz (1979) found that the density neurotransmitters and neurohumors regulate the temporal
of dendritic spines was influenced by monocular deprivation in frameworks as well as sensitivities to external stimuli that are
the visual sensitive period in rats. However, most researchers basic to virtually all sensitive periods.
seem not to measure a system directly, so that in most cases the Examples of neural bases include proposals that maturation
system that is altered in the sensitive period must be inferred. of the visual system in ducklings serves as a pathway in imprint-
This is so, for example, in the influence that gonadal hormones ing (Paulson, 1965), that olfactory cues serve as a pathway for
exert in early development on the eventual expression of sexu- North Pacific salmon to identify their natal tributary (Hasler,
ally dimorphic behaviors in mammals (Reinisch, 1974). As a Scholz, & Horrall, 1978), that perceptual selectivity serves as a
consequence, even the basic nature of targeted systems in sensi- pathway in song learning (Marler & Peters, 1980), and that
tive periods is usually not well worked out. dams' olfactory sensitivity to their own labels on kids serves
Is the system unitary or manifold? Most discussions of sys- as a pathway for maternal responsiveness in goats (Gubernick,
tems subject to sensitive-period analysis proceed as though the 1981).
system were a singular construct. This assumption may be too The sensitive period reflects responsiveness to some stimulus
facile (see Scott, 1986, for a similar suggestion). Very early on, experience outside the organism, takes place at the site of some
Fabricius (1964) argued that imprinting actually involved three system inside the organism, and the stimulus and system con-
independent components for, respectively, eliciting the follow- nect via some pathway. These three material entities define a
ing response, the response itself, and the vigor of the response. second group of structural characteristics fundamental to de-
Recently, Blass (1987) studied the sequence of developing social noting a sensitive period. Nonetheless, many difficult questions
attachments during the nursing period in rats and showed that central to experience, system, and pathway dog investigators of
olfactory social bonding in this system is best understood from sensitive periods. For example, are the presence and absence of
a "multiple" sensitive-periods perspective that includes four in- the stimulus equally or differentially meaningful to the sensitive
dependent yet interrelated processes. period? More elusive—and troubling—is the question of
At what level is the system actually being influenced? Sensi- whether the stimulus is effective in terms of the phenomenology
tive period phenomena may obtain at one or more levels, in- of the organism or as it is defined by the experimenter. Having
cluding prominently the physical, physiological, and psycholog- to infer the system and the pathway can be problematic as well,
ical, and it is often advantageous to specify to which level (or especially since the two are believed to play such central roles
levels) conclusions reached about the nature of sensitive periods in the phenomenon of sensitive periods. For example, insofar
apply. When the kitten experiences a particular visual environ- as the system is altered, it and the functional outcome of the
ment during its sensitive period, what, if any, are the respective sensitive period (see below) could be one and the same, espe-
physical, physiological, and psychological ramifications? Even cially in the short-term. Without distinguishing the two, the ex-
if levels are not directly comparable, it seems necessary to indi- perimenter must remain in the dark as to what was affected
cate at which level or levels change occurs. as opposed to how. Specification of the pathway has clear and
profound implications for understanding the nature of the sen-
Pathway sitive period as well, since manipulation of effects may depend
on a knowledge of the route of those effects. The place of the
The channels by which experience affects the system during pathway in sensitive-period study is therefore important, but
the sensitive period. Pathway designates the physical interface subtle and complex, since even distinguishing the pathway from
between experience and system and is to be distinguished from the system is made difficult when the pathway is somehow also
conceptual questions of how the sensitive period is regulated. altered as the sensitive period unfolds. For these reasons, laying
Pathway is among the least often specified of sensitive-period bare material entities of sensitive periods is key to penetrating
parameters. Either chemical (hormonal) or neural (central ner- their nature.
vous system) pathways have been invoked to describe concrete
ways through which experience and system connect. Some- Consequences
times investigators are able to specify exact means; most times
The third group of parameters concerns later effects of sensi-
they have only been able to infer a means, depending usually on
tive periods. This set includes four structural characteristics as-
a correlation between time course and pattern of susceptibility
sociated with outcomes.
between experience and outcome.
Examples of chemical bases include the proposals that tu-
Outcome
bulin synthesis serves as a pathway of sensitive-period phenom-
ena in kitten cortical visual selectivity (Cronly-Dillon & Perry, The consequence of experience sustained during the sensitive
1976), that testosterone serves as a pathway of sensitive-period period in terms of the normative development of the species.
186 MARC H. BORNSTEIN

What physical, physiological, or psychological aspects of struc- Interpreting Pettigrew's (1978) data on the role of the sensitive
ture or function are influenced by experience during the sensi- period in the ontogeny of binocularity, Aslin (1981) pointed
tive period? Often, the outcome serves as the major source of out that experience may induce or attune development at the
evidence that experience in the sensitive period has in fact had neurochemical level, whereas experience may maintain devel-
a meaningful effect on the organism. Two sets of questions typi- opment at the physiological level.
cally arise with respect to outcome: The first concerns the
sphere of structure or function in which the effect manifests Outcome Conditions
itself, and the second concerns direct or indirect implications of
the outcome for the organism. The temporal and spatial emergence of the outcome following
Sensitive-period phenomena have been hypothesized, and onsets of the sensitive period and of experience. The intercon-
observed, to exert profound effects, sometimes across more nected critical questions that concern outcome conditions of
than one sphere of structure or function, at others within a sin- the sensitive period usually include when and under what cir-
gle sphere. In visual system sensitive periods, outcomes may be cumstances in development the influence of experience mani-
observed in several spheres, as in physical process (Guillery & fests itself relative to the onset of the sensitive period and rela-
Stelzner, 1970), in physiological function (Wiesel & Hubel, tive to the onset of the experience itself.
1963), or in psychological behavior (Ganz & Fitch, 1968; Wie- Is the outcome immediate or eventual? Mitchell and Timney
sel, 1982). Lenneberg (1967) proposed a sensitive period for (1986) reviewed the literature in visual sensitivity and showed
language learning in human beings, supposing the latitude of its that orientation selectivity and binocularity are affected very
outcome to be equally sweeping; in a close analysis of studies soon after the onset of the sensitive period. Marler (1970) re-
intervening in the score of years following Lenneberg's pro- viewed the literature for song learning and showed that vocal
posal, however, Snow (1987) demonstrated that empirical data production often does not emerge until months after the onset
did not support a broad application of the sensitive-period con- of the sensitive period. Immelmann and Suomi (1981) reviewed
cept in language acquisition, but rather confirmed one limited the literature for imprinting and showed that sexual preference
in scope to articulated accent. More usually, outcomes are spe- does not usually emerge until years after the onset of the sensi-
cific to a single sphere of structure or function. For example, tive period.
Brook (1972) found that cell number (and not even cell size) The composition of outcome conditions is not always equiva-
in the adipose organ in humans was the target of a nutritional lently responsive to similar experiences. Money and Annecillo
sensitive period. Moreover, more than a single effect in the same (1987) observed that androgen injected into a pregnant ewe be-
sphere may obtain; an extreme example is handling of rats dur- tween gestational Days 35 and 50 masculinizes the external gen-
ing the sensitive period, which, beyond physiology (Levine & ital anatomy of the lamb, whereas androgen injection after Day
Lewis, 1959), has been observed to manifest itself in a plethora 50 affects only the brain. Moreover, the short-term and long-
of behaviors, including learning (Denenberg & Bell, 1960), ex- term effects of equivalent sensitive-period experiences may be
ploration (Forgays & Read, 1962), and emotional expression similar or they may differ. Bateson (1979) analyzed filial and
(Denenberg, 1963). sexual preferences in finches in this connection. He suggested
The outcome needs further to be defined with respect to its that critical early experience in the sensitive period affects filial
direct or indirect implications for action (Hinde, 1970). For ex- preference in the juvenile period, but exerts effects on sexual
ample, the sensitive period may function for learning a behavior preference in adulthood. Finally, the outcomes of sensitive peri-
necessary for the later performance of that behavior (as is the ods are not always first-order; they can be second-order as well.
following response in imprinting), or it may be necessary for For example, Hirsch and Tieman (1987) pointed out that ner-
some other end (as is smiling for emotional development). vous system changes produced as a developmental outcome of
the sensitive period will systematically influence behavior long
Manner after the sensitive period has closed.

How the influence of experience during the sensitive period Duration


affects the outcome. Experience in the sensitive period may in-
fluence the outcome in several ways. Experience may induce the The temporal nature of the outcome of the sensitive period.
outcome, stimulating the emergence of an effect that would not How long does the outcome of the sensitive period naturally
otherwise ensue; experience may attune the outcome, adjusting endure? As for all other parameters of the sensitive period, the
extant structure or function; or experience may maintain the temporal nature of the outcome doubtlessly depends on many
outcome, continuing the status quo of the system (see Aslin, factors, including which outcome is under scrutiny, in which
1981; Gottlieb, 1983). Oyama (1976) illustrated induction in species, and so forth. Outcomes have normally been presumed
the acquisition of nonnative phonology in the sensitive period to be permanent or, at least, quite long-lived (e.g., Lorenz,
in language learning; by contrast, Wiesel (1982) proposed that 1937). Immelmann (1972) observed that the natural life expec-
innate mechanisms endow the visual system with highly spe- tancy of the zebra finch is less than 7 years. Zebra finches raised
cific connections and that visual experience early in the sensi- by Bengalese finches during the sensitive period for sexual im-
tive period is necessary for the maintenance and full develop- printing have been known to prefer Bengalese finches sexually
ment of cellular connectivity. Of course, experience may oper- after more than 7 years; thus, stability of the imprint seems to
ate to influence outcome in more than one manner: rival the natural life expectancy of the species.
SENSITIVE PERIODS IN DEVELOPMENT 187
The sensitive period is hardly meaningful if it has no conse- months; therefore, cortical cells could be simultaneously
quent in later development or if its consequent is hidden or affected in complex spatial and temporal ways by the interac-
shrouded in mystery—hence the significance of specifying tion of two processes (Daw, Berman, & Ariel, 1978).
structural characteristics associated with antecedent-conse- Separate sensitive-period characteristics also vary depending
quent relations, such as outcome, manner, outcome conditions, on known species differences. Immelmann and Suomi (1981)
and duration. Even though antecedent-consequent relations reported that the duration of the sensitive period for sexual im-
must be among the sensitive period's most conspicuous charac- printing is longer in the Bengalese finch than it is in the zebra
teristics, many unanswered questions persist about outcomes. finch. Henry (1984) studied the susceptibility of auditory func-
For example, when the outcome is displaced in time from the tion to environmental noise in two genetically distinct strains
sensitive period, its boundary definitions are clear; but how are of mice and found that 133 C57BL/6 mice have a sensitive pe-
system and outcome distinguished when the two are closely co- riod for acoustic priming only, whereas 183 CBA mice have a
ordinate in space and time? Further, is an outcome normative sensitive period for acoustic priming for audiogenic seizures.
for the species? Imprinting shows that the outcome of typical Belyaev et al. (1985) reported that the offset of the sensitive pe-
experience encountered during the sensitive period will be nor- riod for primary socialization in farm-bred silver foxes takes
mative. However, outcomes may be anomalous. Teratogen place at 40-45 days, but for comparable foxes selected for do-
effects demonstrate equally clearly that an outcome may be mesticated behavior the offset of the sensitive period takes place
highly atypical for the species. at 60-65 days. Since it is to be expected that individuals nor-
mally give different but discrete values for a sensitive-period
Evolutionary and Ontogenetic Time Scales characteristic, it is important to note that the group function
for a characteristic may be abrupt and representative of individ-
Qualitative and quantitative estimates for every sensitive-pe- uals or it may appear continuous and fail to represent individual
riod structural characteristic can be expected to vary naturally; data.
in addition, many parameters will be modifiable based on expe- Different species may differ in quantitative details of an anal-
rience or experiment. Thus, in describing all of the foregoing ogous sensitive period; such differences are often quite informa-
structural characteristics of the sensitive period, it is necessary tive. The following studies exemplify interspecific variation in
to consider two generic properties, variability and modifiability. developmental timing, in triggering stimulus, and in the exis-
tence of a sensitive period. The Japanese quail develops rapidly
Variability and is already adult-like by about Week 3, and its sensitive pe-
riod for sexual imprinting takes place within that time (Gal-
The range and causes of variation within and among species lagher, 1977); by contrast, the domestic fowl chick develops over
in developmental dating, onset, offset, duration, asymptote, ex- a much longer period, and its sensitive period for sexual im-
perience, and pathway of a system during the tenure of the sensi- printing takes place at a correspondingly later time (Vidal,
tive period, and the range and causes of variation in outcome, 1975). Redhead ducks imprint on visual and auditory stimula-
manner, outcome conditions, and duration of the outcome for tion provided by the mother, by contrast, canvasback ducks,
a given system's sensitive period subsequently. What are the their close cousins, imprint more strongly on auditory stimula-
population's central tendency and distribution values for the tion alone (Mattson & Evans, 1974). Most dramatically, rhesus
several characteristics of a sensitive period? In the absence of monkeys that do not experience interaction with peers in the
systematic study, it is impossible to say with assurance what the first 9 months of life later have difficulty establishing peer rela-
nature of the distribution of values for sensitive-period parame- tionships (Harlow & Harlow, 1969); by contrast, pigtail mon-
ters may be, although it is generally reasonable to expect popula- keys that are raised under similar circumstances of social depri-
tion values to adhere to a normal distribution. Two central is- vation exhibit many fewer interpersonal difficulties later (Sack-
sues arise with regard to variability; they concern, first, varia- ett, Holm, & Landesman-Dwyer, 1975).
tion in each sensitive-period characteristic within a species and, Are these dispersions meaningful? Within species, variability
second, variation across species for each sensitive-period char- seems to reflect expected genetic dispersion or functional
acteristic. differences; across species, the distribution of sensitive-period
Research documents different kinds of variation in sensitive- characteristics seems to be adjusted to species-appropriate de-
period parameters within a species. Scott (1958), for example, velopmental timetables and conditions of rearing. Beyond their
estimated the variability in onsets of sensitive periods for social naturally occurring variability, sensitive-period characteristics
behavior of puppies at 3-4 days on either side of the species may be experientially or experimentally modifiable.
mean value. Variation can also be found at different levels of
system function. Wiesel (1982), for example, observed that Modifiability
temporal parameters of sensitive periods for cortical vulnera-
bility vary among types of deficit, among brain regions, and The degree to which developmental dating, onset, offset, dura-
among layers within individual cortical areas. Taking note of tion, asymptote, experience, and pathway of a system may be
such variation is nontrivial, since sensitive-period effects may altered during the tenure of the sensitive period, and the degree
interact with one another. For example, the sensitive period for to which outcome, manner, outcome conditions, and duration of
orientation selectivity in kittens ends at about 1.5 months, and the outcome may be altered subsequently, as well as the age-
the sensitive period for binocular selectivity ends at about 2 graded nature of their flexibility. Sensitive periods are custom-
188 MARC H. BORNSTEIN

arily thought of as rigid and refractory to change, but research system? Is modifiability naturally occurring, must it be in-
shows that many sensitive-period characteristics are modifi- duced, or is it an epiphenomenon of non-natural testing proce-
able. For example, cells in the cortex of the very young kitten dures? What factors influence the modifiability of sensitive-pe-
are subject to sensitive periods for orientation selectivity and riod parameters?
for binocularity, but the duration of those periods can be ex- A particularly thorny issue with respect to modifiability turns
tended by dark rearing (e.g., Cynader, Berman, & Hein, 1976; on the question of how incompleteness or impermanence of
Mower & Christen, 1985), as it can be reduced (or eliminated) outcome impact on credibility and investment in the idea of the
by depletion of relevant neurotransmitters (e.g., Daw, Rader, sensitive period. Normally, either can be expected to be very
Robertson, & Ariel, 1983); the sensitive period can also be rein- damaging. Lenneberg (1967), for example, who postulated a
stated in older cats by the infusion of noradrenalin (Pettigrew, sensitive period for learning language, argued that normal lan-
1982). Likewise, the sensitive period for filial imprinting in guage acquisition depends on normal language experience be-
chicks and in ducks can be extended by chemical means (Hess, tween approximately 2 and 14 years of age; yet startling contra-
1957), by selective perceptual experience (Moltz & Stettner, dictory examples, such as Kaspar Hauser in Nuremberg, Ger-
1961), or by social rearing conditions (Sluckin, 1972), and it many, who acquired language after the age of 17 years (Simon,
can be prevented altogether by stress (Landsberg & Weiss, 1979) and Genie in California who began to acquire language
1975). Modifiability is not limited to sensitive periods specific after the age of approximately 14 years (Curtiss, 1977), cast gen-
to early life; the sensitive period for maternal interest in neonate uine doubt on the strong form of Lenneberg's hypothesis (see
lambs can be altered when parturition in ewes is chemically Snow, 1987). That effects of a sensitive period are not fixed need
induced (Poindron et al., 1979), it can be prolonged by maternal not, however, undermine the notion of the sensitive period, so
social isolation (Moore, 1960), and it can be reopened by genital long as something special for development from that period re-
stimulation (Keverneetal., 1983). mains. Thorpe's (1961) classic work on song learning in the
Fixity of outcome is likewise widely thought to be one of the chaffinch is illustrative: The fledgling male chaffinch that hears
sensitive period's most salient characteristics (e.g., Lorenz, adults singing, or as a juvenile sings itself, will later produce
1937). To many minds, the sensitive period's lasting effect is the characteristic adult song, even if competition for territory is
what stamps this phenomenon with its special character. later required for adumbration of the fine details of its song.
Among the many aspects of the sensitive period, the perma- Utopian modifiability opens a door otherwise shut tight by re-
nence of effects has been intensively investigated (and chal- lentlessly strict interpretation of the sensitive period.
lenged; see Clarke & Clarke, 1976), presumably on account of
the important role this eventuality would play in verifying the Overview
nature and significance of the sensitive period in the first place.
Some outcomes do indeed seem to endure permanently. For ex- However diverse and specialized their elected subjects of in-
ample, exposure to one range of ambient temperatures early in vestigation, researchers of sensitive periods implicitly seem to
development leads to masculinization of turtles, whereas expo- recognize, first, the existence, function, and prominence of sev-
sure to another range leads unalterably to feminization (Bull, eral characteristics of the sensitive period and, second, the req-
1980). Research has shown, however, that many sensitive-pe- uisiteness of specifying their quantitative and qualitative
riod outcomes are modifiable or even reversible. Isolation in makeup. Essentially, therefore, a comprehensive statement
the first 12 months of the monkey's life eventuates in severely about a sensitive period ought ideally to include information
maladjusted social behaviors (Harlow & Harlow, 1969); how- about its temporal and intensive contours: (a) when and how
ever, "therapy" at a later time (including adaptation, self-paced often in the life cycle the sensitive period occurs, (b) the rise of
visual input, and exposure to younger normal monkeys) can the sensitive period, (c) the decay of the sensitive period, (d) the
ameliorate adverse effects to a degree and encourage more ap- window of the sensitive period, and (e) how sensitivity changes
propriate species-normal behaviors (Novak & Harlow, 1975). and the stability of sensitivity; about its mechanisms of change:
Outcomes may be differentially mutable depending on the (f) the nature and origins of the effective experience, (g) what
level of the system affected. Both anatomy (e.g., Olson & Free- structure or function changes, and (h) the channels by which
man, 1978) and behavior (e.g., Timney, Mitchell, & Griffin, experience affects the structure or function that changes; and
1978) in the cat can be altered by visual deprivation in the sensi- about its consequences: (i) the outcome in later development,
tive period, but both may "recover" in the wake of stimulation (j) how the outcome is effected, (k) when and under what cir-
in the post-sensitive-period period (see, too, Blasdel, Mitchell, cumstances the outcome occurs, and (1) how long the outcome
Muir, & Pettigrew, 1977). By contrast, psychological systems of lasts. Beyond these defining parameters of the sensitive period
behavior in rats appear to recover from stress by handling or by and its consequences, information about two evolutionary and
shock more quickly and completely than do physiological ones ontogenetic considerations of sensitive periods is also requisite:
(Ader, 1968; Levine & Lewis, 1959). (m) individual and species variation in sensitive-period charac-
Structural characterisitics of the sensitive period seem not to teristics and (n) the modifiability of the individual parameters
be fixed, but generically vary and are modifiable. With respect of the sensitive period.
to the refractory nature of sensitive-period characteristics, Thus, 14 conceptually distinct structural characteristics ar-
many additional questions linger, such as How modifiable are rayed in four groups can be identified as inhering in the sensitive
individual sensitive-period parameters? Does modifiability period. All researchers confront the task of describing each of
vary at different developmental points in the life course of the these characteristics; indeed, many view the quantitative delin-
SENSITIVE PERIODS IN DEVELOPMENT 189

cation of some or all of these parameters to be a primary goal life of an organism—certainly before the conscious, self-aware
of studying sensitive periods. Indeed, descriptive specification selection of experiences. That is, the plasticity that inheres in
of characteristics constitutes a first-order achievement of sensi- the concept of the sensitive period has a distinctly negative con-
tive-period study; additionally, it is critical to illuminating strual, too. The second evolutionary ramification of the sensi-
causes underlying sensitive-period phenomena. tive period is, then, the jeopardy to the organism introduced by
the sensitive period. Conditions that are necessary to or typical
A Sensitive Period Framework: of development but that are not met, or atypical conditions that
II. Causal Interpretations are encountered haphazardly, place the organism at permanent
risk. The sensitive period is, therefore, poised to facilitate adap-
Next to designating characteristics that define its structure, tation or to handicap the unsuspecting organism perhaps for
the aspect of the sensitive period that challenges, entices, and the remainder of its existence. Indeed, the original discoveries
perplexes developmental investigators most is the task of iden- of sensitive periods were based on the permanent damage
tifying causes underlying its emergence. Questions of cause di- caused by noxious stimulation during early phases in develop-
vide into two classes: The first asks why the sensitive period ment. For these reasons, sensitive periods offer especially ab-
arises, and the second asks how specifically the sensitive period sorbing subjects of study.
is regulated. The sensitive period confronts researchers and the- In many ways, sensitive periods improve in comprehensibil-
oreticians working in different systems with a conceptually and ity when contemplated as a form of adaptation. Like all adapta-
evolutionally enigmatic phenomenon to explain on each of tions, even analogous sensitive periods can be expected to vary
these two levels, and one in which the significance of intricate in their particular manifestations among species on account of
and complex factors such as nature, nurture, and their transac- the different histories of natural selection of those species. How-
tion through time are clearly at issue. Interpretations of the evo- ever, a given sensitive period can be expected to be universal
lutionary meaning of sensitive periods vary (the Why? ques- within a species principally because of shared evolutionary (ge-
tion), as do attributions of sources by which sensitive periods netic and environmental) history.
are regulated (the How? question). A comprehensive treatment Ethologists, particularly, have concerned themselves with ad-
of the sensitive period at the descriptive level (the What? ques- dressing the question of why sensitive periods arise. In doing so,
tion) is requisite to addressing these two deeper concerns about ethologists speculate on the twin foundations of survival and of
cause. In this section, I discuss these two foremost questions reproductive success of organisms that inhabit different niches
about cause of the sensitive period in seriatim. (e.g., Baker, 1938; Thomson, 1950), and sensitive periods have
figured prominently among their speculations in this regard. It
Ultimate Cause: Why Evolutionally may be that ultimate causes of sensitive periods are selected for
do Sensitive Periods Arise? in the natural history of the organism and eventuate as specific
adaptations. Consider the case of ungulates; "herds of grazing
The sensitive period reflects a developmental phase of built- mammals characteristically produce precocial offspring in syn-
in competence for specific exchange between organism and chrony, and it is therefore important for the mother to form a
environment whose consequences presumably endure for the rapid recognition of her own offspring to distinguish them from
organism. Thus, the sensitive period qua evolutionary mecha- others" (Pissonnier et al., 1985, p. 361).
nism represents a psychological phenomenon of singular conse- Immelmann and Suomi (1981) have viewed the sensitive pe-
quence. There are two perspectives from which it is necessary riod out of such an evolutionary perspective, accounting
to view the evolutionary meaning of the sensitive period. The thereby for species variation in parameter values of many struc-
first is constructive and positive: The sensitive period uniquely tural characteristics of sensitive periods. Consider, for example,
prepares the system for its developmental future, forecasting the duration parameter, \bung animals must acquire critical
mature structure or function relative to early experience. The social knowledge from conspecifics before departing the family,
sensitive period thereby ensures that the system is responsive to and therefore sensitive periods for learning social behaviors
its developmental environment, and it buffers the system must fall within those chronological bounds when the young of
against later change in the environment or in the self. Such a a given species are still with their parents. Avian species as a
powerful and pervasive ontogenetic mechanism presumably re- whole spend considerably less of their developmental history af-
flects a beneficial adaptation within the evolutionary program ter birth with their parents than do mammals, and therefore it
of the organism. For this reason, perhaps, most sensitive periods is predictable that avian sensitive periods for the acquisition of
are to be found in the infancy of the organism, since their ap- social knowledge are shorter lived than are mammalian ones
pearance at this time safeguards that the organism will quickly and that the population variation for sensitive-period duration
and completely acquire information that is both critical to and among birds is more restricted than it is among mammals. As
typical of its physical and social locale. This is practical infor- Immelmann and Soumi (1981) point out,
mation that is commonly thought to enhance the probability of
survival and the achievement of adaptive competence. In this In many species and for different functional systems, strong selec-
construal, the sensitive is an "optimal" period. tion pressures that favor great sensitivity to certain environmental
stimuli and a maximum of learning during early stages of life may
The sensitive is also a "vulnerable" period, however, since in well exist. They may also favor great stability of the results of such
the sensitive period brief experiences can exert profound and early experience, providing some kind of degree of protection
sometimes permanent detrimental effects from very early in the against some later possible influences on the individual. In addi-
190 MARC H. BORNSTEIN

tion, it becomes apparent that differences in such specific needs and through close examination of biomolecular phenomena. Rein-
demands between species are almost certainly responsible in large isch (1974) showed that hormones (specifically androgens)
part for the enormous diversity in the degree of stability and in the
duration and characteristics of sensitive phases, (p. 399, emphasis function critically during the sensitive period of brain organiza-
added) tion to influence a wide variety of sexually dimorphic behav-
iors, and Landsberg and Weiss (1976) showed that hormones
On this account, it behooves researchers always to consider the (specifically blood corticosterones) play a determinative role in
sensitive period they study out of an evolutionary perspective, the sensitive period for filial imprinting among young precocial
since adopting such an outlook promises to enrich investiga- birds. Indeed, Lauder and Krebs (1986) have inferred that neu-
tors' understanding of individual structural characteristics rotransmitters and neurohumors act as general mechanisms
through the larger meaning of the sensitive period for the species underlying all sensitive periods.
in question. In short, the evolutionary stance helps to unravel
some mysteries about why sensitive periods might arise as Physiological
well as why they possess some of the particular characteristics
they do. Regulation of characteristics of the sensitive period through
physiological mechanisms, including variation in state of
Proximate Cause: How are Sensitive Periods Regulated? arousal, anatomy, or perceptual capacity. Different investiga-
tors have argued for the pivotal contribution of each of these
Adaptive consequence aids in attributing ultimate cause of physiological mechanisms, even with respect to the same class
a sensitive period in a species. However, there also must exist of sensitive period. For example, in imprinting among young
corresponding "proximate cause" that regulates sensitivity to precocial birds, Martin and Schutz (1974) determined that gen-
meet the aim of natural selection for the sensitive period. Exam- eral arousal played a significant role; Strobel, Baker, and Mac-
ination of proximate cause addresses the question of how sensi- Donald (1967) and Bradley (1985) that change in central ner-
tive periods are regulated. vous system structures played a significant role; and Immel-
To confirm attributions of proximate cause is exacting. Un- mann (1972) that advances in visual perceptual ability played
derstandably, pinpointing the mechanism of a natural interac- a significant role.
tion, such as the sensitive period, challenges investigators con-
ceptually. Moreover, signal confounds of empirical designs typi- Psychological
cal of much research into sensitive periods have thrown up
special obstacles against fitting causal inference. Only system- Regulation of characteristics of the sensitive period through
atic experimentation can clarify the nature of cause and bring psychological mechanisms, including prominently variation in
explicitness to deductions so common and seemingly necessary behavior. Activities of the organism itself may influence the sen-
to theorizing about the sensitive period. Happily, Bateson and sitive period. Hess (1973) established that locomotion plays a
Hinde (Bateson, 1979, 1983; Bateson & Hinde, 1987; Hinde & determinative role during the sensitive period for filial imprint-
Bateson, 1984) have outlined three classes of proximate cause ing among precocial birds; Freeman and Bonds (1979) demon-
explanation for the sensitive period and delineated for each per- strated that eye movements are decisive in the sensitive period
missible limits of causal attribution. I recount each in turn, for cortical binocularity in the kitten; Gubernick (1981) discov-
modifying the original terminology somewhat to accord with ered that mother goats' licking their young is necessary during
the vocabulary established in this article. the sensitive period for olfactory recognition of offspring; and
The alteration in individual responsiveness that betokens the Gottlieb (1985) confirmed that embryonic ducks must produce
sensitive period can logically reflect regulation by physical, their own contact-contentment call during a sensitive period in
physiological, or psychological mechanisms. These three classes order to exhibit a normal preference for the species-specific ma-
of mechanism may operate in concert, and presumably differ- ternal call.
ent mechanisms account for different categories of sensitive pe- Elucidating mechanism in proximate cause is vital as it re-
riods in different proportions. veals how and why, among other things, sensitive periods arise,
endure, and decay. However, at least three interrelated caveats
Physical must be heeded in attributing proximate cause in a sensitive
period to one or more mechanisms; this triad concerns exclu-
Regulation of characteristics of the sensitive period through sivity, reductionism, and temporal priority among mecha-
physical mechanisms, including variation in genetics and bio- nisms. First, although physical, physiological, and psychologi-
molecular process. One way in which researchers have at- cal levels of explanation may be distinguished operationally, the
tempted to identify genetic mechanisms of cause, for instance, attribution of causality to one or another mechanism can be
is by contrasting differences in sensitive periods across related confounding, since these levels of cause are by no means mutu-
species. Freedman (1967) showed that distinct strains of dogs ally exclusive. Molecular status of the system can underpin be-
react qualitatively differently following a sensitive period for havioral change that initiates a sensitive period, but behavioral
handling, and Henry (1984) showed that distinct strains of mice change can equally well induce molecular change that instigates
experience qualitatively different sensitive periods to audio- the behavioral change. For example, naturally maturing levels
genie seizures. A second way researchers have attempted to as- of corticosterones have been implicated in the development of
say physical mechanisms that regulate sensitive periods is fear, which in turn influences imprinting; perhaps, however,
SENSITIVE PERIODS IN DEVELOPMENT 191

naturally occurring stressors provoke corticosterone produc- nation of both immediate mechanism and adaptive meaning.
tion, or experience with novelty produces stress, and so on. In Clearly, insights into proximate cause along with indications of
short, the attribution of causality in proximate cause is poten- ultimate cause enlarge the scope of understanding of sensitive
tially subject to a critique of circularity. It may be safest to con- periods. However, achieving unabridged intuition about causes
ceive of causes of a sensitive period as layered. of sensitive periods poses a true challenge.
A second correlated caveat concerns the seductive, but rather
simplistic, reductionism that often tempts hypothesizing about Implications of the Sensitive Period Framework
proximate cause in sensitive-period research. In this orienta- for Research and Theory
tion, psychological attributions immediately invoke explana-
tions in terms of physiological substrates—perceptual function How can attending to descriptive features and explanatory
is reducible to cortical status—just as physiological attributions meaning lead to advances in theoretical and empirical research
immediately invoke explanations in terms of physical sub- in individual sensitive periods or in the sensitive period generi-
strates—cortical plasticity is reducible to neurohormonal flow. cally? Systemization of research efforts around these character-
Researchers must be ever vigilant to acknowledge and to respect istics of structure and interpretations of cause presents certain
the integrity of each class of mechanism. clear advantages. In this section, I discuss how the foregoing
A third associated caution in attributing proximate cause is organization contributes to understanding sensitive periods,
that a given mechanism may apply at the time the sensitive pe- and in doing so I provide both concrete and theoretical exam-
riod actually arises, or it may apply from an earlier time. For ples that show how new insights might be secured from the
example, physiological mechanisms could engender a sensitive framework described.
period in a system immediately, or physiological mechanisms Research designs that dominate published investigations of
could prepare a system for later instigation of the sensitive pe- sensitive periods—independent of content area—nearly uni-
riod. Inevitably, ambiguity must be expected in distinguishing formly are devoted to specifying one or another of the several
immediate cause from cause displaced in the past. As a conse- structural characteristics of the sensitive period. (Proximate
quence of these several considerations, assigning monistic prox- and ultimate cause have generally provoked less attention.) Rel-
imate cause in the domain of the sensitive period is extremely evant literatures abound with specific examples of both obser-
hazardous. It ought to be possible to do so theoretically, how- vational and experimental investigations of nearly every char-
ever, even if the various categories of proximate cause are not acteristic. In the typical experimental design, investigators ma-
restricted. To achieve greater insight into the pertinence of one nipulate values of one parameter, holding (some) other
or another explanation of the sensitive period, it appears to be parameters constant (to the degree possible), in order to deter-
both desirable and feasible to contrast explanations of different mine the meaningful range of values for the single parameter of
mechanisms experimentally. If, for example, programmed interest. So, for example, in an experimental series a neuropsy-
physical factors excite a sensitive period, the system ought to chologist interested in the sensitive period for visual sensitivity
display altered responsiveness independent of associated psy- might first expose groups of animals to the same visual experi-
chological expression. ence at different times in their ontogeny and later assess the in-
Perhaps the most pervasive, penetrating, and elusive question fluence of developmental dating on anatomy, physiology, or be-
regarding proximate cause of the sensitive period recalls the havior in order to evaluate the parameter of developmental dat-
Nature-Nurture debate (and has equally much meaning): Is ing of the sensitive period. In subsequent experiments, the
proximate cause endogenously, exogenously, or interactively in- neuropsychologist might expose groups of animals during that
fluenced? Opinions on this question vary dramatically. Con- newly defined sensitive period to different visual experiences,
sider the variety of interpretations that have been offered to ac- holding duration of exposure constant, or for different dura-
count for the offset of the sensitive period in imprinting: Expla- tions of exposure, holding the experience itself constant, in or-
nations include perceptual maturation (Moltz, 1968); the der to evaluate the critical nature of the experience and its dura-
emergence of fear, itself brought about by inherent age-related tion in the sensitive period. Other permutations are self-
forces (Hoffman, 1987; Lorenz, 1935; Scott, 1962; Weiss, evident.
Kohler, & Landsberg, 1977) or by social experience (Alley & Insofar as examining each of the 14 parameters of the sensi-
Boyd, 1950; Salzen, 1963); and new objects in the environment tive period (to say nothing of cause) may require numerous sep-
(Sluckin, 1964) or other nonspecific photic stimulation (Milli- arate groups or treatments, exhaustive study is often not possi-
kan, 1972); as well as the process of imprinting itself (Guiton & ble or might not be deemed worthwhile. In practice, research
Sluckin, 1969). By turns, too, the phenomenon of the sensitive investigators rarely meet the considerable challenge of specify-
period itself has received a similarly diverse theoretical treat- ing parameter values even for a plurality of the 14 characteris-
ment. Gottlieb (1961) argued that sensitive periods arise out of tics of the sensitive period they study.
endogenous motives; Hess (1973) argued that sensitive periods However, failure to explore certain parameters comprehen-
arise on account of exogenous factors; and Bateson and Hinde sively, or to recognize the need to explore them in depth, has led
(1987) argued that sensitive periods arise ineluctably from the to consequential differences of opinion or of fact about sensitive
interaction of endogenous with exogenous forces (see, too, periods, and thereby limited understanding of this phenome-
Bronson, 1962, 1965; Over, 1979; Schneirla & Rosenblatt, non. Consider the following examples. First, on account of the
1963). primacy, speed, rapidity, and permanence of the social attach-
The explication of cause of a sensitive period calls for exami- ments precocial ducklings were observed to form, Lorenz
192 MARC H. BORNSTEIN

(1937) identified and described imprinting as a "critical pe- into a uniform view of the phenomenon of the sensitive period
riod."2 Systematic investigation of structural characteristics as- per se.
sociated with imprinting subsequent to Lorenz led to quantita- Despite this striking diversity among individual instances of
tive modification of his qualitative attributions about several sensitive periods, the proposed research framework lends itself
aspects of the nature of imprinting—and, not insignificantly, to to the profitable establishment of common quantitative values
reversals of Lorenz's pronouncements on the abruptness, the for the several parameters of sensitive periods and of sound
uniqueness, and the permanence of these time-bound attach- qualitative intuition about cause. In this regard, what specific
ments. advantages does the taxonomy afford? Dividing the sensitive pe-
Second, it is widely assumed that the sensitive period reflects riod into constituent processes enables their individualized
an individually unique phenomenon normally circumscribed study and imparts a higher order of understanding both to con-
to an early phase of the life-cycle. Yet, phylogenetic study dis- stituents themselves and to the sensitive period as a whole. Con-
closes multiple sensitive periods for maternal bonding in a sub- sider, for example, developmental dating, a prime sensitive-pe-
stantial number of adult mammals (Rosenblatt & Siegel, 1981). riod structural characteristic. The sensitive period for binocu-
Not only are these findings revolutionary with respect to the larity has been found to keep between postnatal Weeks 4 and
common view of the sensitive period, but such a perspective in 12 in the cat (e.g., Hubel & Wiesel, 1970), Months 1 and 2 in
turn opens a range of rather novel questions about the sensitive the monkey (e.g., Wiesel, 1982), and Years 1 and 7 in the human
period. For example, if sensitive periods are multiple, rather being (e.g., Banks et al., 1975). By themselves, each of these
than singular, in the individual, has the sensitive period a refrac- values provides meaningful species information, but a deeper
tory period? Is there one, or are there several separate, maternal explication of sensitive-period mechanisms is gained through
sensitive periods for twin births? more comprehensive species comparison, since comparative
Third, parameter values of sensitive periods must be appreci- developmental dating reveals that in each species the sensitive
ated to fluctuate, reflecting different experimental approaches period for binocularity appears to initiate approximately when
and different empirical indexes. Thus, for example, the fine- cells driven by each eye are matured sufficiently to compete for
grainedness of analysis places limits on specifying the develop- cortical synapses, and the sensitive period in each appears to
mental timing of visual system sensitivity; behavioral data sug- cease approximately when competitive synaptogenesis stabi-
gest one parameter value for offset of the sensitive period in lizes (see, e.g., Kasamatsu & Pettigrew, 1979; Wiesel & Hubel,
language deprivation, whereas physiological data suggest an- 1963).
other; and, the experiences of isolated versus communal rearing Additionally, having a unified framework within which to
considerably alter variability in imprinting. study sensitive periods enables knowledge garnered in one sub-
Fourth, based on earlier demonstrations that showed han- ject area to be applied to others. For example, sensitive periods
have been observed normally to occur very early in the ontoge-
dling in a critical period affected rats' later behavior (Denenberg
netic history of many systems in many species, that is during
& Zarrow, 1971), Wyly, Denenberg, de Santis, Burns, and Zar-
prenatal development or infancy. The organizational perspec-
row (1975) examined the rabbit for the existence of an analo-
tive imported here has two notable implications for thinking
gous critical period. Unlike the rat, the rabbit does not display
about this aspect of the sensitive period. First, the standard re-
especial sensitivity in open-field, exploratory, or social behavior
sult suggests that, in searching for sensitive periods in any new
in response to handling early in its infancy, but rather exhibits
system, it might be strategically efficient initially to focus on
selective effects that have proved cumulative rather than time-
the early life course of that system. Such an approach can be
locked. Clearly, cross-species evaluations inform both specific
expected to reduce the risk of missing and to enhance the likeli-
and general comprehension of the sensitive period. hood of detecting a sensitive period. The literature in infantile
Last, the obligatory reliance on correlational techniques and stimulation provides an illustration. Bernstein (1952) observed
natural experiments in human sensitive-period research has that animals that experienced more handling in adolescence
sometimes misled conclusions. For example, Lenneberg (1967) gained more weight in full maturity and performed in a supe-
speculated that the effects of language deprivation would rever- rior manner on discrimination tasks compared with adolescent
berate immutably in the child's inability to acquire and to use animals handled minimally or not at all. Later, on the basis of
language with facility; however, Lenneberg failed to examine general experience in sensitive-period research, Hunt and Otis
examples that would test his speculations about the duration of (1963) and Schaefer (1963) reasoned—it turned out cor-
deprivation. Extant case histories, as of Kaspar Hauser, should rectly—that such outcomes might be enhanced if animals were
have given pause to the strong claims for a sensitive period in first handled in their infancy rather than their adolescence.
human language acquisition. The second implication of a general finding is that anomalous
On their face, sensitive periods vary bewilderingly both in or contradictory results may flag close scrutiny. The question of
locus and in time: hours for ducklings to imprint (e.g., Hess, a sensitive period for maternal bonding in human beings illus-
1973), days for birds to learn a song (e.g., Marler, 1970), weeks trates the point (Klaus & Kennell, 1976). Certainly, confirma-
for canine socialization (e.g., Scott, 1962), months to ensure
sexual normalcy in monkeys (e.g., Harlow & Harlow, 1969), 2
Not insignificantly, Lorenz's actually calling the phenomenon he
and years in the case of human binocular sensitivity (e.g., Banks observed a "critical" period imbued it with a host of unnecessary con-
et al., 1975). This variety seems understandably, if unhappily, notations that many of his heirs, in the exact same and in conceptually
to have daunted researchers and to have masked intelligence related fields, have had to struggle (thanklessly) to rectify and overturn.
SENSITIVE PERIODS IN DEVELOPMENT 193

tion of a sensitive period for maternal bonding in infrahuman Whatever their subfield, investigators of sensitive periods
species intimates that it exists in human beings. In spite of how confront similar challenges, because sensitive periods sui gene-
extraordinary and commanding an experience the birth of a ris are described by a common set of characteristics and require
child may be, claims for a systemic sensitive period for maternal similar kinds of explanation. On these bases, a framework of
bonding at parturition among human beings ought still to have description and explanation in sensitive-period research has
been greeted with more reserve, simply on the argument that crystallized. A central purpose of articulating this framework is
the timing of sensitive periods is almost always localized to in- to foster broader and deeper quantitative and qualitative treat-
fancy rather than to maturity. In this example, the framework ments of sensitive periods in future. Clearly, too, the principles
instigates search cum skepticism. A sensitive period for adult of sensitive periods clarified by students of one system can be
anything constitutes a low probability event a priori, and— serviceable to students of other systems. Yet, many investiga-
claims and desires to the contrary—contemporary research has tors seem genuinely unaware of the relevance to their own work
largely failed to substantiate the existence of a sensitive period of sensitive periods subjected to investigation in allied fields;
for bonding in humans (see reviews by Goldberg, 1983; Her- indeed, some research and write as though oblivious to other
bert, Sluckin, & Sluckin, 1982;Leiderman, 1981; Myers, 1984). manifestations of the phenomenon. This strategy needlessly
Arriving at this conclusion does not mean that parameter val- jeopardizes advances in comprehending individual sensitive pe-
ues outside general norms are unobtainable or nonexistent; a riods and the sensitive period in general.
sensitive period for maternal bonding can be found in some in- No sensitive period in one system must resemble that in any
frahuman species (Rosenblatt & Siegel, 1981; Pissonnier et al., other, and no one sensitive period need serve as a model for
1985). Rather, it suggests that investigators can and ought to others. There is no all-encompassing theory of the sensitive pe-
avail themselves of common parameter values growing out of riod, although many investigators and theoreticians have
the research framework to predict and to evaluate new as well searched for one. It is possible, nonetheless, to advance a frame-
as existing findings. Reciprocally, however, researchers are wise work of structural characteristics and causal interpretations out
to refrain from exclusive reliance on such strategizing, as it may of which to consider sensitive periods generally. In other words,
prove overly conservative. To continue the example at hand, one "sensitive period" does not mediate cortical specificity and
wholly depending on general experience risks the potential re- filial imprinting; but a unified framework might still apply
ward to be reaped, say, from discovering a novel or unique sensi- across the full spectrum of remarkably variegated instantia-
tive period specific to mature phases of the life-cycle. tions of sensitive periods. In turn, that framework will prove to
Lucid and extensive description are practically imperative be a rewarding heuristic tool toward redefining both philosophy
with phenomena as disparate and intricate as sensitive periods. and experiment in sensitive-period research.
The more articulate and learned the characterization, the more Elucidating such a universal framework for the sensitive pe-
likely is the researcher to gain a deeper comprehension of the riod has been the task of this commentary. Conceptual analysis
sensitive period. Sensitive periods constitute unique windows and research review suggest that investigators of sensitive peri-
of organism-environment interaction, positive or negative as ods who wish to grasp the essence of this ubiquitous develop-
their consequences may be. To the extent that the sensitive pe- mental phenomenon thoroughly are obliged, first, to acknowl-
riod concept has relevance to biology, psychology, and sociol- edge parameter values of 14 different structural characteristics
ogy, not enough information can ever be gleaned about its struc- of the sensitive period, as they are embedded in four distinctive
tural characteristics and causal interpretations. Clear and com- conceptual sets, and, second, to appreciate both ultimate cause
prehensive description is vital to accessible research. The of the sensitive period in terms of its adaptive significance and
purpose of the framework delimited here is to bring order to the proximate cause of the sensitive period in terms of mechanisms
complexity and diversity inherent in sensitive period study. that might regulate the sensitive period. Perhaps no existing re-
port of a sensitive period—the undeniable popularity of this
Conclusion phenomenon in many areas of biological, psychological, and so-
ciological science notwithstanding—meets the task of specify-
Despite its contemporary heterogeneity and high degree of ing all structural characteristics and causal interpretations. As
specialization, psychology embraces many general phenomena demonstrated, however, the movement toward a comprehensive
that are of broad interest across its subdisciplines. This is true, treatment promises invaluable direction to all future inquiry.
in part, because of the generality and ubiquity of those phenom- In the end, unfortunately, even this detailed and extensive
ena. The sensitive period in development qualifies as one. Many framework will fail to provide information that is exhaustive
examples have emerged in widely different structural or func- and determinative. Even where there may be widespread empir-
tional systems that the presence or absence of certain experi- ical agreement about values to be attached to sensitive-period
ences at particular times in the life-cycle may influence struc- characteristics, and some indications of ultimate and proximate
ture or function well beyond the time of the experience. Exam- cause may offer themselves, theoretical convergence about the
ples of sensitive periods may be found widely dispersed in conceptual sources of sensitive periods may still be lacking. For
animal and in human neurobiology and behavior. Proof of the example, different theoretical traditions propose different rea-
extraordinary breadth and rewarding character of the concept sons why sensitive periods tend to occur early in ontogeny. Mat-
of the sensitive period is that it has been applied profitably to urational theory argues that the period of greatest susceptibility,
explicating development of cells, of human beings, and of insti- vulnerability, or responsiveness to stimulation in an organiza-
tutions. tional process coincides with the phase of its most rapid growth,
194 MARC H. BORNSTEIN

usually early in the life-cycle; information theory posits that Belyaev, D. K.., Plyusnina, I. Z., & Trut, L. N. (1985). Domestication
systems in a state of developmental flux, as is usually true of in the silver fox (Vulpes fulvus Desm): Changes in physiological
early ontogeny, are more open to external influences than are boundaries of the sensitive period of primary socialization. Applied
organized and fixed systems; learning theory suggests that ac- Animal Science, 13, 359- 370.
Bernstein, L. (1952). A note on Christie's "Experimental naivete and
quisition proceeds most efficaciously when there are no extant experiential naivete." Psychological Bulletin, 49, 38- 40.
competing responses, the situation that necessarily character- Blakemore, C., & Mitchell, D. E. (1973). Environmental modification
izes the earliest life stage of a system; and, cognitive develop- of the visual cortex and the neural basis of learning and memory.
mental theory proposes that mature and complex capacities are Nature, 241, 467-468.
constructed of simple elements that themselves develop first in Blasdel, G. G., Mitchell, D. E., Muir, D. W., & Pettigrew, J. D. (1977). A
infancy. Thus, even when the framework of the sensitive period physiological and behavioral study in cats of the effect of early visual
is adequately detailed, inmost facets of sensitive periods will re- experience with contours of a single orientation. Journal of Physiol-
main enigmatic and unattainable. ogy, 265,615-636.
Sensitive periods appeal to developmental investigators for Blass, E. M. (1987). Critical events during sensitive periods of social
many reasons—from the superficial attraction of what has been development in rats. In M. H. Bornstein (Ed.), Sensitive periods in
called the "pleasing dactylic rhythm" of the term itself to the development: Interdisciplinary perspectives (pp. 81-98). Hillsdale,
NJ: Erlbaum.
"exciting connotation of developmental brinksmanship" the
Boothe, R. G., Vassdal, E. & Schneck, M. (1986). Experience and devel-
phenomenon connotes. Despite this power, sensitive periods opment in the visual system: Anatomical studies. In W. T. Greenough
should not enjoy a license to rivet the developmentalist's atten- & J. M. Juraska (Eds.), Developmental neuropsychobiology (pp. 295-
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time in the life-cycle of a system may exert a dramatic effect on disciplinary perspectives. Hillsdale, NJ: Erlbaum.
the future developmental course of that system. Research shows Bradley, P. (1985). A light and electron microscopic study of the devel-
that events subsequent to the sensitive period may intervene to opment of two regions of the chick forebrain. Developmental Brain
modify or even nullify effects thus established, or it may be in Research, 20, 83-88.
the character of the system itself to modulate at later points in Bronson, G. (1962). Critical periods in human development. British
its life history. As is widely recognized, every phase in the life Journal of Medical Psychology, 35, 127-133.
course is somehow critical. Still, to paraphrase the poet, theory Bronson, G. (1965). The hierarchical organization of the central ner-
vous system: Implications for learning processes and critical periods
and data signify that some periods in life may be more critical in early development. Behavioral Science, 10, 7-25.
than others. Brook, C. G. D. (1972, September 23). Evidence for a sensitive period
in adipose-cell replication in man. Lancet, 2, 624-627.
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