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First-Rank Symptoms in Schizophrenia: Reexamining Mechanisms of

Self-recognition
Flavie A. V. Waters* and Johanna C. Badcock
Centre for Clinical Research in Neuropsychiatry, Graylands
Hospital, Australia; School of Psychiatry and Clinical
Neurosciences, The University of Western Australia, Perth
Disturbances of self are a common feature of schizophrenic
psychopathology, with patients reporting that their
thoughts and actions are controlled by external forces,
as shown in rst-rank symptoms (FRS). One widely ac-
cepted explanatory model of FRS suggests a deciency
in the internal forward model system. Recent studies in
the eld of cognitive sciences, however, have generated
new insights into how complex sensory and motor systems
contribute to the sense of self-recognition, and it is becom-
ing clear that the forward model conceptualization does not
have unique access to representations about the self. We
briey evaluate the forward model explanation of FRS,
reassess the distinction made between the sense of agency
and body ownership, and outline recent developments in 4
domains of sensory-motor control that have supplemented
our understanding of the processes underlying the sense of
self-recognition. The application of these ndings to FRS
will open up new research directions into the processes un-
derlying these symptoms.
Key words: psychosis/self/agency/body ownership/
internal forward model/sensory-motor
Introduction
Anomalies of self-experiences are a critical feature of
schizophrenia-spectrum disorders. First-rank symptoms
(FRS), particularly, are considered to be at the core of
schizophrenia psychopathology.
1
FRS refer to experien-
ces whereby thoughts and actions are perceived to be un-
der the control or influence of an external agent or where
there is a loss of clear boundaries between the sense of self
and others. In contemporary research classifications,
a subset of FRS are typically examined, frequently
referred as passivity experiences (see table 1). People
experiencing FRS suffer from deficits in self-recognition
because they have difficulties distinguishing between self
and others and are unsure whether thoughts and actions
are separate and independent from external influences.
FRS are intriguing because they raise questions about
how the human mind is able to make a distinction be-
tween self and nonself. Unraveling the processes that
underlie these symptoms has relevance beyond the imme-
diate theoretical implications for schizophrenia by shed-
ding some light on the human abilities that form the basis
of all communication and socialization.
FRS play a key role in the diagnosis of schizophrenia
and feature prominently in current diagnostic systems.
The growing literature on FRS reflects the renewed inter-
est in their cognitive and neural processes
2,3
and their di-
agnostic significance.
4,5
FRS, however, are not easily
explained in terms of traditional neuropsychological dys-
function,
6
and the pathophysiological mechanisms un-
derlying these symptoms continue to elude researchers.
One widely accepted explanatory model of FRS suggests
a dysfunction in the internal forward model system.
7,8
The model suggests that the ability to differentiate be-
tween the self and others is rooted in motor control pro-
cesses and that FRS arise because of faulty action
processing mechanisms. This model has produced inter-
esting findings but has tended to dominate experimental
research into FRS. There has been a paucity of empirical
investigations questioning this view, despite accumulat-
ing evidence that the forward model does not provide
a definite answer to FRS. In addition, recent studies in
the field of cognitive sciences have generated new insights
into how complex sensory and motor systems contribute
to the sense of self-recognition. Studies reveal, firstly, that
there are many different, overlapping, representations of
the self that are not exclusively tied to the motor system
and, secondly, that there is a range of cues available to
recognize the self that have yet to be individually exam-
ined in patients with FRS. For the purpose of this over-
view, we adopt a broad definition of self-recognition,
namely the recognition of the self as an entity indepen-
dent from others and as an agent of behavior, given
*Corresponding author: Dr Flavie Waters, Centre for Clinical
Research in Neuropsychiatry, Graylands Hospital, Mail Bag No 1,
Claremont, Perth, 6910, Australia. tel: 61 8 9347 6429, fax: 61 8
9384 5128 (Flavie@ccrn.uwa.edu.au)
Schizophrenia Bulletin vol. 36 no. 3 pp. 510517, 2010
doi:10.1093/schbul/sbn112
Advance Access publication on August 27, 2008
The Author 2008. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved.
For permissions, please email: journals.permissions@oxfordjournals.org.
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that concepts and terms referring to this area of inquiry
often overlap.
In the current article, we briefly evaluate the forward
model explanation of FRS and review recent advances in
4 areas of sensory-motor control that have supplemented
our understanding of the mechanisms of self-recognition
inhealthy people. These newresearchdirections may guide
future investigations into the processes that underlie FRS.
Forward Model Framework
The forward model is a theoretical model of cognitive
motor control, whose role consists in predicting the sen-
sory consequences of motor commands. This predictive
process allows the differentiation of sensations occurring
as a result of intentional movements from sensations
originating from changes in the external world.
912
The
ability to distinguish between these sensations arises be-
cause the forward model anticipates, and diminishes, the
sensory effects occurring as a result of self-generated
movements. The internal system deduces from dimin-
ished sensory effects that sensations have arisen from
a motor command that we issued. By contrast, sensations
that are externally produced are experienced more
strongly and are interpreted to have an external cause.
Friths proposal
7,8
is that patients with FRS are unable
to predict internally the perceptual consequences of their
actions so that the salience of sensations is not dimin-
ished, resulting in actions being perceived to be externally
generated. Forward model abnormalities are also
thought to predict difficulties in self-monitoring of willed
intentions and actions, and deficits in detecting and
correcting errors during self-generated movements.
Jeannerod
13,14
has recently expanded on the forward
model by proposing an action simulation framework.
The proposal not only retains the idea that the motor sys-
temuses internal forward models, but it also suggests that
internal systems compute different kinds of representa-
tions for first-person and third-person information that
enable self-/other distinctions and external attributions.
One difficulty facing FRS research is their heterogene-
ity in presentation, which includes abnormalities of
thoughts, action, perception, and emotions. To account
for this diversity, the forward model makes the 2 further
assumptions: (1) that FRS represent one core dimension
related to cognitive motor control, resting on the idea
Table 1. First-Rank Symptoms (Passivity Symptoms) in Schizophrenia
Symptom Denition
a
Patients Description
b
Third-person auditory
verbal hallucinations
Voices which have no real origin in the outside
world and which the patients regard as
separate from their own mental processes.
Voices speak about or comment on the patient.
I hear the voice of my stepfather saying
he never gets anything right. The voice
of God says to me she is the only one who
can save us now.
Loud (audible) thoughts Patients report that their own thoughts seem so
loud that someone near by could hear them.
I can hear myself think. Loud enough for
another to hear.
Thought insertion Thoughts are experienced as not being the patients
own. Often, the alien thoughts are perceived to
have been inserted from outside by an external
agent.
Some thoughts are not my own. They belong
to Satan: He types in evil thoughts about
killing people. People are stufng around
in my mind, putting thoughts inside.
Thought broadcast Patients experience their thoughts as accessible to
others, sometimes diffusing out of their mind, so
that the content of the patients mind is no
longer private.
Other people can know my thoughts. I am not
able to feel any privacy.
Thought withdrawal Patients report that their thoughts have been taken
out of their minds. The thoughts are experienced
to be actively extracted by others.
Satan rips out, pulls out, brings out the
thoughts out of my soul. It feels like that.
My thoughts get stolen.
Made experiences/
replaced control of will
Actions, intentions, and/or feelings are experienced
to be under the control of some other force.
Often, patients believe that someone elses words
are coming out using their voice or that their
movements are being willed by some outside
power and that their personal intention has
been replaced by the sense that some other
is in control.
Someone makes me move my mouth, my jaw,
and pushes the words out. I cant help
but say something.
Im forced to walk around, Im being made
to turn right and left.
I dont have control over my feelings any
more, how I react to emotions now is not the
same as before I entered the house of ghosts.
a
Based on the Schedules for Clinical Assessment in Neuropsychiatry (SCAN) definitions.
72
b
Waters et al.
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that thoughts and actions are all instances of intentional
behaviors ranging from the covert (mental activities)
to the overt (actions)
13
and (ii) that these phenomena
and behaviors are subject to the same constraints as
motor processes and consequently that the outcome of
a disorder in motor control, notably in forward model-
ing, comprises anomalies spanning the entire range of
human experiences.
In summary, the forward model suggests that the sense
of self is underpinned by a complex multistage motor
control system. A dysfunction in this system is thought
to be responsible for creating the self-disturbances shown
in patients with FRS.
Evidence of Forward Model Dysfunction in FRS
Evidence cited in support for the forward model frame-
workincludes studies showing that schizophrenia patients
withFRSdemonstrate abnormalities insensations arising
from intentional movements, as shown on a task measur-
ing responses toself-producedtactile sensations (tickles)
15
andona taskassessing the cancellationof retinal informa-
tion during smooth eye pursuit.
16
Studies have also dem-
onstrated abnormalities in self-monitoring mechanisms,
suchas failing tocorrect a wrong movement inthe absence
of visual feedback.
17,18
Patients with FRS also show dif-
ficulties when making decisions based on whether the
visual feedback of an action corresponds to their own
movements, or to another person, as demonstrated on
self-/other attribution tasks,
19,20
and in remembering
the origin of verbal material in memory.
21,22
Several limitations, however, are impeding an evalua-
tion of the strength of the association between a forward
model dysfunction and FRS. For instance, many studies
have reported forward model impairments in the broader
schizophrenia population without reference to FRS, so
that the association of these deficits to FRS specifically
remains under question. Other methodological limita-
tions in the literature include (1) inconsistency, or lack
of transparency, concerning which symptoms are tar-
geted during the patient selection process, (2) small sam-
ple sizes, and (3) inclusion of nonpassivity phenomena
(such as delusion of mind reading) in FRS categorization.
Another limitation is the use of a recruitment criterion
based on the presence of only one FRS. Given the het-
erogeneous nature of FRS, and in view of the risks of in-
correctly identifying these symptoms, studies may reach
incorrect conclusions by indexing symptoms other than
FRS. A recruitment criterion based on the presence of
at least 2 FRS might provide a more reliable categoriza-
tion method. A suitable comparison group may include
patients with no lifetime history of FRS.
Theoretical aspects of the model have also attracted
criticism.
2326
For example, questions have been raised
concerning the correct interpretation about the conse-
quence of a forward model dysfunction, given that for-
ward model deficits may account for the feeling of not
being in control of ones actions but not for the experi-
ence that a separate agent is controlling these actions.
24
In addition, Blakemore et al
27
have showed that the feel-
ing of not being in control is not necessary to generate
the belief that ones actions are controlled by external
forces. Also, a complete failure of the forward model
would result in broad deficits in motor control, while
studies have shown that forward model processes for
low-level automatic action control seem to be unim-
paired in schizophrenia.
28
Few studies of FRS, however, have considered that the
forward model conceptualization is only one of several
sources of informationthat contribute to self-recognition.
One possible reason comes from the prevalent view that
patients with FRS have a disordered sense of agency
but an intact sense of body ownership. This has resulted
in an almost unilateral research focus on motor control
processes in FRS.
Sense of Agency and Body Ownership
The observation that patients with FRS do not have the
sense of causing their movements and frequently misat-
tribute their own actions to another agent has led to the
proposal that FRS reflect a disturbance in the sense of
agency.
8,24,29,30
By contrast, patients with FRS appear
to have a preserved sense of their own body, resulting
in the proposal that they have an intact sense of body
ownership. The terms have been given different defini-
tions, but the sense of agency may be defined as the sense
that one is in control of ones actions or the sense an
agent has that he or she is the author of that action.
31
This differs from the sense of body ownership, which
refers to a sensory awareness of the body that is not ex-
clusively tied to actions. Tsakiris et al
32
have defined
body ownership as the special perceptual status of
ones own body, which makes bodily sensations seem
unique to oneself. In this conceptualization, the sense
of agency is intrinsically associated with, and secondary
to, action execution and therefore linked to the motor
control system. By contrast, body ownership is tied to
the combination of sensory experiences arising from the
body senses, as well as internal information about the
bodys position at all times.
The theoretical differences between the sense of agency
and body ownership have attracted much interest,
33
but
several lines of evidence are now challenging the view
that patients with FRS have a selective deficit in the sense
of agency. To start with, the sense of body ownership and
thesenseof agencyare not modular anddiscrete but may, in
fact, be interdependent and overlapping.
31,3436
For exam-
ple, the computation of action processes contributing to
a sense of agency relies critically on body ownership proc-
esses, suchas coherent multisensorysignals arisingfromthe
same body parts, as well as internal spatial body represen-
512
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tations. The body senses and position of the limbs are also
constantly being updated during the bodys interaction
withthe environment, andthis continuouslychanging state
of reference is used by the forward model to recalibrate
its predictions about the state of the system and to differ-
entiate betweenself- andother-generatedsensations,
26,33,37
demonstrating the interdependence of body ownershipand
agency processes.
Deficits on attribution tasks shown in patients with
FRS, in which patients are asked to identify a movement
as belonging to the self or to another person based on
video visual feedback,
19,20
have also been cited as evi-
dence of a selective impairment in the sense of agency.
However, performance on these tasks necessarily requires
an implicit knowledge of ones body as a sensory object
that is moving (ie, a sense of body ownership), so that
attribution deficits may also reflect a disturbance in
body ownership.
38
In addition, low-level perceptual def-
icits in combining visual and somatosensory (ie, nonmo-
tor) signals from the same body parts may also affect the
ability to judge accurately whether an action has been
performed by the self or by another person, so that an
explanation based on sensory deficits may also account
for attribution errors. Conversely, the ability to make ref-
erence to the sense of body ownership actually involves
making a self-attribution judgment,
38
which therefore
does not only arise from a sense of agency. Altogether,
this suggests that the concepts of agency and body
ownership are intrinsically linked and cannot be fully
dissociated.
Philosophical discussions have also been helpful in for-
mulating aspects of self-experiences. For instance, phe-
nomenological descriptions of the experiential self have
proposed levels of selfhood that are hierarchically orga-
nized and overlapping.
3941
Briefly, there are different
forms of selves, starting from a very basic notion of
the self that is prereflective and determined by an implicit
and sensory awareness of first-person experience. This
form of self-awareness may be linked to the body owner-
ship experience. By contrast, the sense of agency may be
tied to a more explicit and reflective formof the self that is
consciously defined as I. Finally, there is a more com-
plex level of selfhood that is composed of social and per-
sonal characteristics. Importantly, these various levels of
selves are entwined and cannot be observed in isolation
from each other.
Furthermore, a dissociation between the sense of
agency and body ownership has yet to be tested unequiv-
ocally in schizophrenia patients with FRS. Instead,
phenomenological examinations have pointed out that
patients with schizophrenia suffer from disturbances in
the sense of self that extend beyond the domain of action
awareness, comprising the entire field of self-experiences
including abnormalities in the sense of body owner-
ship.
23,42
In sum, there is a need for experimental studies
to challenge the views that FRS arise exclusively because
of a dysfunction in motor control processes, and that they
are essentially a disorder of agency.
Cues Underlying Self-recognition
A different approach to understanding the processes that
contribute to self-recognition has consisted in using
healthy people to examine how the self is inferred, utiliz-
ing experimental paradigms in which self-distortions are
experimentally manipulated. The cues examined refer to
body ownership processes (sensory integration and body
schema), motor control subcomponents (efferent motor
signals), and subjective psychological experiences. While
the forward model includes many of these signals as con-
stituent processes in its proposal, the critical point is that
the studies reviewed below demonstrate that these cues
contribute in their own unique way to the sense of
self-recognition. This means that the sense of self is nei-
ther exclusively linked to a combination of processes tied
to the motor systemnor is it secondary to action execution,
so that deficits in nonmotor processes can also result in
abnormalities of self-experiences. Consequently, the for-
ward model formulation, as it is conceptualized, does not
have sole access to representations about the self.
Importance of Sensory Integration
While the forward model emphasizes the role of motor
feedback and programming, new research is showing
that processes extending beyond intentional motor pro-
cesses are also important contributors for a sense of
self.
13,4346
For instance, recent studies have highlighted
the importance of the successful integration of multiple
sensory signals arising from the external environment.
Matching visual and somatosensory input from the
same body parts are critical for building a coherent image
of our body, as shown in experimental paradigms where
inducing a sensory conflict is sufficient to produce a dis-
sociation in the sense of self. In one such study, a set of
rubber hands is placed in a position that is compatible
with the participants posture, while the participants
hands are out of view. Watching brush strokes applied
to the rubber hands while feeling synchronous strokes
on ones arm induces the feeling that the rubber hand
is part of the participants own hand.
44
These results sug-
gest that altered self-experiences can arise as a result of
conflicting/incongruent sensory signals. In the same
way, out-of-body experiences may be created experimen-
tally simply by manipulating the senses.
45,47
Ehrsson
45
re-
cently conducted an experiment in which people watched
an illusory image of themselves through virtual-reality
goggles that projected an image of themselves from the
back. When the experimenter stroked the persons
back at the same time as projecting the image of a plastic
rod stroking the illusory body, participants reported the
feeling of watching themselves from the back. That is,
513
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their sense of self had transported itself outside their
physical body, so that participants experienced watching
another persons body in ones own body. These experi-
ments demonstrate a critical role for multisensory inte-
gration in assisting perceptual decisions about self-
recognition and show that a mismatch between visual
perspective and proprioceptive signals is enough to in-
duce disturbances in self-experiences. Importantly, there
was no intentional motor component involved in the par-
adigm, suggesting that intentions do not have privileged
access to representations of self, contrary to the assump-
tions of the forward model.
Role of Body Schema
The body schema is a dynamic spatial coding of the body,
its internal organization, boundaries, and relationships.
48
It is an internal frame of reference about the structure and
position of the body, and it is thought to be important for
enabling self-recognition. The body schema is also used
to coordinate actions and to allow fluid movement
through space by providing a representation of the
body parts at all times with respect to each other.
49
Cos-
tantini and Haggard
50
demonstrated the importance of
internal limb representations arising from the body
schema using the rubber hand illusion. Specifically, spa-
tial mismatches between the participants hand posture
and the rubber hand posture were created by rearranging
either the subjects hands or the rubber hands to be at
odds with each other. It was revealed that the body illu-
sion was strongest when the image of the rubber hands
matched the participants existing representation of their
own body and lowest when the rubber hands position
did not correspond to the subjects actual hand positions,
underlining the importance of preexisting internal body
representations. The authors argued that these represen-
tations are needed to provide a spatial context in which to
assimilate novel sensory information and constrain mo-
tor commands. Importantly, by providing this frame of
reference about existing internal body representations,
the body schema is thought to contribute to the aware-
ness of ones own body and actions and to the discrim-
ination of self fromothers. The body schema is, therefore,
intimately related to self-recognition.
Importance of Efferent Motor Signals
The forward model proposes that the sense of self is sec-
ondary to action execution, yet another point of view
argues that efferent (motor) commands play a more spe-
cific role toward self-recognition.
32,51,52
Tsakiris et al
51
used a self-recognition paradigm in which subjects could
see their right hand as an image via video feedback, while
the hand was passively moved either by the subjects left
hand or by the experimenter. The results showed that
self-recognition was at chance level if only proprioception
was available (when the hand was moved by the experi-
menter), whereas the added efferent information (when
the participant made his own hand move) significantly
increased self-recognition performance. The authors
interpreted the results as suggesting that efferent signals
provide more critical cues in enabling self-recognition
than proprioception alone, arguing against the forward
model proposal that a cohesive sense of self only occurs
after sensory feedback. The role of efferent signals was
further examined in a manipulation of the rubber hand il-
lusion in which both passive and active finger movements
were used.
32
In the passive condition, the illusion was lo-
calized only to the area that was stimulated (the finger). By
contrast, when active finger movements were used, the il-
lusion extended to the whole hand suggesting that efferent
motor commands integrated different body parts into
a wider awareness of the body in action. The authors pro-
posed that efferent motor signals contribute to the sense of
self-recognition by enabling a global subjective awareness
of all limbs involved in movement. Importantly, as pointed
out by Schwabe and Blanke,
53
this means that the role of
the forward model goes beyond attenuating sensations of
the moving body part by affecting a more global represen-
tation of the body in a very complex way.
Role of Psychological Binding Effects
A related area of research has shown that there are sub-
jective effects of actions that also contribute to the under-
standing of how self-recognition is inferred.
5458
For
example, recent studies from Haggard and colleagues
55,56
have shown that when a voluntary action is followed by
an expected sensory consequence, a psychological bind-
ing effect occurs so that these events are perceived to have
occurred closer together in time than they actually did. In
other words, this intentional binding effect refers to the
subjective perception that cause and effects are drawn to-
gether in perceived time. Haggard has argued that this
temporal shrinkage between intentional actions and their
behavioral effects creates an experience of causation be-
tween actions and their consequences, thus enhancing
our feeling of self-authorship. From the idea that inten-
tions play a critical role in representing our movements,
the authors argue that self-recognition is inferred from
this enhanced subjective experience of intentionality.
Furthermore, this temporal binding effect is thought to
be sensitive to top-down influences associated with motor
intentions, suggesting that psychological experiences of
anticipated actions have distal effects on sensory-motor
perception and that expectations may play a critical role
in representing our movements.
Summary and Discussion
Proponents of the internal forward model suggest that
a disorder in the system that predicts the sensory conse-
514
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quences of ones actions may result in a disordered sense
of self, as in FRS. However, recent developments in the
area of sensory-motor control have shown that a model
based on motor feedback and programming does not
fully account for the clinical and experimental data
and that there are several additional cues that contribute
to self-recognition: there is a need for consistent and co-
herent signals across the body senses, as well as informa-
tion about body location and orientation provided by the
body schema. The role of purely efferent motor com-
mands has also been readdressed and is now thought
to contribute to body representations by providing
a broad subjective sense of our limbs in movement. In
addition, it is becoming clear that intentional actions pro-
duce the subjective experience that willed actions and
their external consequences are related, as shown when
voluntary movements and their effects are perceived to
have shifted toward each other in time.
Sensory integration and body schema are areas of re-
search that remain to be fully examined in schizophrenia
patients with FRS, but there are indications that these
processes may be impaired in this patient group. For ex-
ample, a study by Peled
59
showed that schizophrenia
patients felt the rubber hand illusion stronger and faster
than normal controls, although the results were not ex-
amined in relation to symptom clusters. More recently,
Farrer and Franck
60
used a modified version of an action
attribution task that involved rotated visual feedback of
hand postures. They reasoned that if patients with FRS
have body ownership impairments, they would show in-
creased attribution impairments as the rotation in-
creased. The authors found that both patient groups
with and without FRS made more errors across all con-
ditions compared with a nonclinical control group. Al-
though there were no significant differences between
patient groups, and no effect of rotation, patients with
FRS actually tended to make more errors across all
conditions than patients without these symptoms and
controls. This points to difficulties in matching the
congruence of tactile and visual signals and deficits in
body ownership processes in FRS patients. These
results are consistent with studies showing body
schema impairments in the wider schizophrenia popula-
tion.
61
In sum, there are indications that multisensory
integration and body schema may be impaired in schizo-
phrenia. Future studies should examine this pattern of
performance in FRS patients specifically. Purely efferent
motor signals also remain to be investigated in this pa-
tient group.
There has recently been evidence of an association be-
tween impaired intentional binding and schizophrenia,
with patients showing excessive binding between inten-
tional actions and their sensory consequences (Haggard
et al, 2003). It was suggested that this contracted sense of
time might result in an erroneous perception of action
causation and in particular to abnormal action attribu-
tion in schizophrenia patients with self-disturbances.
However, no symptom analysis was conducted, so the as-
sociation between impaired action timing and FRS still
remains to be tested. However, there is evidence of timing
impairments extending beyond overt motor control in
schizophrenia patients with FRS as shown on a task of
motor imagery
62,63
and on an auditory discrimination
task requiring judgments of temporal intervals.
64
Given
the role of timing precision for shaping the sensory
awareness of movements
65
and for generating the subjec-
tive perception that some events belong together,
55
these
abnormalities in timing awareness in patients with FRS
may contribute to a breakdown in the perceived relations
between actions and their effects. How this fits exactly in
relation to other processes involved in self-recognition is
yet to be determined.
In summary, we have demonstrated that there are
several sources of information that contribute to self-
recognition. They are not evidence against the forward
model framework, given that sensory signals, efferent mo-
tor information, expectations, and timing are all constit-
uent parts of the model. However, the above studies show
that a motor control theory reliant on a combination of
these cues overlooks their unique contribution for en-
abling self-representations. We have also argued against
theprevailingviewthat FRSareevidence of aselective def-
icit in the sense of agency because evidence suggests that
the sense of agency and body ownership are intrinsically
linked and cannot be observed in isolation from each
other. Given the lackof clear separation betweendifferent
forms of selves, FRS should perhaps be viewed as reflect-
ing an altered sense of self-experience (rather than im-
paired agency).
One last comment about the above research is that it
has focused almost exclusively on self-recognition of
body experiences and actions. There are concerns
24
that other forms of intentional experiences, especially
thoughts, cannot be reduced to sensory-motor processes
and that we must look elsewhere for an explanation.
One parallel but important stream of research demon-
strates the importance of cognitive and social contribu-
tors to the sense of self-recognition.
6670
These studies
have developed independently of research on sensory-
motor processes but share the idea that intentions
are important for retrospective inferences about self-
recognition. They provide an alternative perspective
on mental phenomena that are not easily accommo-
dated by sensory-motor constructs, although it should
be noted that some studies have not supported the pro-
posal that intentions are necessary for representing the
self.
45,64
A reexamination of the role of intention might
therefore provide important clues to the abnormalities
underlying FRS.
Finally, while the processes underlying self-recognition
are slowly unraveling, the brain mechanisms contributing
to the subjective experience that some behaviors are un-
515
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der external control still remain to be identified. These are
core experiences in schizophrenia and must remain an ac-
tive area of inquiry.
Funding
National Health and Medical Research Council Austra-
lian Research Training Fellowship (404117 to
F.A.V.W.).
Acknowledgments
We are grateful to Prof Assen Jablensky for providing
comments on this article.
References
1. Schneider K. Klinische Psychopathologie. Stuttgart, Germany:
Georg Thieme Verlag; 1950.
2. Ceccherini-Nelli A, Turpin-Crowther K, Crow T. Schneiders
first rank symptoms and continuous performance disturbance
as indices of dysconnectivity of left- and right-hemispheric
components of language in schizophrenia. Schizophr Res.
2007;90:203213.
3. Posada A, Franck N, Augier S, Georgieff N, Jeannerod M.
Altered processing of sensorimotor feedback in schizophre-
nia. C R Biol. 2007;330:382388.
4. Jansson L, Parnas J. Competing definitions of schizophrenia:
what can be learnt from polydiagnostic studies? Schizophr
Bull. 2007;33:11781200.
5. Nordgaard J, Arnfred S, Handest P, Parnas J. The diagnostic
status of first-rank symptoms. Schizophr Bull. 2007;34:137
154.
6. Waters FAV, Badcock JC, Milan D, Jablensky A. Neuropsy-
chological functioning in schizophrenia patients with first-
rank (passivity) symptoms. Psychopathology. In Press.
7. Frith CD, Blakemore SJ, Wolpert DM. Abnormalities in the
awareness and control of action. Philos Trans R Soc Lond B
Biol Sci. 2000;355:17711788.
8. Frith CD. The neural basis of hallucinations and delusions. C
R Biol. 2005;328:169175.
9. Blakemore SJ, Frith CD. The role of motor contagion in the
prediction of action. Neuropsychologia. 2005;43:260267.
10. Kelso J. Planning and efferent components in the coding of
movement. J Mot Behav. 1977;9:3347.
11. Sperry R. Neural basis of spontaneous optokinetic responses
produced by visual inversion. J Comp Physiol Psychol.
1950;43:482489.
12. Wolpert DM, Ghahramani Z, Joardan MI. An internal model
for sensorimotor integration. Science. 1995;269:18801882.
13. Jeannerod M. The mechanism of self-recognition in humans.
Behav Brain Res. 2003;12:115.
14. Jeannerod M. Being oneself. J Physiol (Paris). 2007;101:161
168.
15. Blakemore SJ, Smith J, Steel R, Johnstone EC, Frith CD. The
perception of self-produced sensory stimuli in patients with
auditory hallucinations and FRS: evidence for a breakdown
in self-monitoring. Psychol Med. 2002;30:11311139.
16. Lindner A, Their P, Kircher TT, Haarmeier T, Leube DT.
Disorders of agency in schizophrenia correlate with an inabil-
ity to compensate for the sensory consequences of actions.
Curr Biol. 2005;15:11191124.
17. Frith CD, Done D. Experiences of alien control in schizo-
phrenia reflect a disorder in the central monitoring of action.
Psychol Med. 1989;19:359363.
18. Turken A, Vuilleumier P, Mathalon D, Swick D, Ford J. Are
impairments of action monitoring and executive control true
dissociative dysfunctions in patients with schizophrenia? Am
J Psychiatry. 2003;160:18811883.
19. Daprati E, Franck N, Georgieff N, et al. Looking for the
agent: an investigation into consciousness of action and
self-consciousness in schizophrenic patients. Cognition. 1997;
65:7186.
20. Franck N, Farrer C, Georgieff N, et al. Defective recognition
of ones own actions in patients with schizophrenia. Am J
Psychiatry. 2001;158:454459.
21. Keefe RSE, Arnold MC, Bayen UK, McEvoy JP, Wilson
WH. Source monitoring deficits for self-generated stimuli in
schizophrenia: multinomial modeling of data from three sour-
ces. Schizophr Res. 2002;57:5167.
22. Woodward TS, Menon M, Hu X, Keefe RSE. Optimization
of a multinomial model for investigating hallucinations and
delusions with source monitoring. Schizophr Res. 2005;85:
106112.
23. Cermolacce M, Naudin J, Parnas J. The minimal self in
psychopathology: re-examining the self-disorders in the
schizophrenia spectrum. Conscious Cogn. 2007;16:703714.
24. Gallagher S. Neurocognitive models of schizophrenia: a -
neurophenomenological critique. Psychopathology. 2004;37:
819.
25. Pacherie E, Green M, Bayne T. Phenomenology and delu-
sions: who put the alien in alien control? Conscious Cogn.
2006;15:566577.
26. Synofzik M, Their P, Lindner A. Internalizing agency of self-
action: perception of ones own hand movements depends on
an adaptable prediction about the sensory action outcome. J
Neurophysiol. 2006;96:15921601.
27. Blakemore SJ, Oakley DA, Frith CD. Delusions of alien con-
trol in the normal brain. Neuropsychologia. 2003;41:1058
1067.
28. Delevoye-Turrell Y, Giersch A, Danion JM. Abnormal
sequencing of motor actions in patients with schizophrenia:
evidence from grip force adjustments during object manipula-
tion. Am J Psychiatry. 2003;160:134141.
29. Gallagher S. Philosophical conceptions of the self: implica-
tions for cognitive science. Trends Cogn Sci. 2000;4:1421.
30. Graham G, Stephens G. When Self-consciousness Breaks:
Alien Voices and InsertedThoughts. Cambridge, MA: MITPress;
2000.
31. Pacherie E. The sense of control and the sense of agency.
Psyche. 2007;13:130.
32. Tsakiris M, Prabhu G, Haggard P. Having a body versus
moving your body: how agency structures body-ownership.
Conscious Cogn. 2006;15:23432.
33. Tsakiris M, Schutz-Bosbach S, Gallagher S. On agency and
body-ownership: phenomenological and neurocognitive
reflections. Conscious Cogn. 2007;16:645660.
34. Kircher T, Leube D. Self-consciousness, self-agency, and
schizophrenia. Conscious Cogn. 2003;12:656669.
35. Legrand D, Brozzoli C, Rossetti Y, Farne A. Close to me:
multisensory space representations for action and pre-
516
F. A. V. Waters & J. C. Badcock

b
y

g
u
e
s
t

o
n

J
u
l
y

6
,

2
0
1
4
h
t
t
p
:
/
/
s
c
h
i
z
o
p
h
r
e
n
i
a
b
u
l
l
e
t
i
n
.
o
x
f
o
r
d
j
o
u
r
n
a
l
s
.
o
r
g
/
D
o
w
n
l
o
a
d
e
d

f
r
o
m

reflexive consciousness of oneself-in-the-world. Conscious
Cogn. 2007;16:687699.
36. Sadler J. The psychiatric significance of the personal self. Psy-
chiatry. 2007;70:113129.
37. Legrand D. The bodily self: the sensori-motor roots of pre-
reflexive self-consciousness. Phenomenol Cogn Sci. 2006;
5:89118.
38. Bulot V, Thomas P, Delevoye-Turrell Y. Sense of agency: ex-
periencing is not judging. Encephale. 2007;33:603608.
39. Zahavi D, Parnas J. Phenomenal consciousness and self-
awareness: a phenomenological critical of representational
theory. J Conscious Studi. 1998;5:687705.
40. Sass L, Parnas J. Schizophrenia, consciousness and the self.
Schizophr Bull. 2003;29:427444.
41. Parnas J, Handest P. Phenomenology of anomalous self-
experience in early schizophrenia. Compr Psychiatry.
2003;44:121134.
42. Parnas J, Handest P, Jansson L, Sbye D. Anomalous subjec-
tive experience among first-admitted schizophrenia spectrum
patients: empirical investigation. Psychopathology.
2005;38:259267.
43. Balslev D, Cole J, Miall RC. Proprioception contributes to
the sense of agency during visual observation of hand move-
ments: evidence from temporal judgements of action. J Cogn
Neurosci. 2007;19:15351541.
44. Holmes NP, Snijders HJ, Spence C. Reaching with alien
limbs: visual exposure to prosthetic hands in a mirror biases
proprioception without accompanying illusions of ownership.
Percept Psychophys. 2006;68:685701.
45. Ehrsson H. The experimental induction of out-of-body expe-
riences. Science. 2007;317:1048.
46. Van den Bos E, Jeannerod M. Sense of body and sense of
action both contribute to self-recognition. Cognition.
2002;85:177187.
47. Lenggenhager B, Tadi T, Metzinger T, Blanke O. Video ergo
sum: manipulating bodily self-consciousness. Science.
2007;317:10961099.
48. Schwoebel J, Coslett H. Evidence for multiple, distinct repre-
sentations of the human body. J Cogn Neurosci. 2005;17:543
553.
49. Maravita A, Spence C, Driver J. Multisensory integration
and the body schema: close to hand and within reach. Curr
Biol. 2003;13:R531R539.
50. Costantini M, Haggard P. The rubber hand illusion: sensitiv-
ity and reference frame for body ownership. Conscious Cogn.
2007;16:229240.
51. Tsakiris M, Haggard P, Franck N, Sirigu A. A specific role
for efferent information in self-recognition. Cognition.
2005;96:215231.
52. Tsakiris M, Haggard P. Experimenting with the acting self.
Cogn Neuropsychol. 2005;22:387407.
53. Schwabe L, Blanke O. Cognitive neuroscience of ownership
and agency. Conscious Cogn. 2007;16:661666.
54. Engbert K, Wohlschlaeger A, Thomas R, Haggard P.
Agency, subjective time, and other minds. J Exp Psychol
Hum Percept Perform. 2007;33:12611268.
55. Haggard P, Clark S, Kalogeras J. Voluntary action and con-
scious awareness. Nat Neurosci. 2002;5:382385.
56. Haggard P. Conscious intention and motor cognition. Trends
Cogn Sci. 2005;9:290295.
57. Linser K, Goschke T. Unconscious modulation of the conscious
experience of voluntary control. Cognition. 2007;104:459475.
58. Sato A, Yasuda A. Illusion of sense of self-agency: discrep-
ancy between the predicted and actual sensory consequences
of actions modulates the sense of self-agency, but not the
sense of self-ownership. Cognition. 2005;94:241255.
59. Peled A. Touch-feel illusion in schizophrenia patients. Biol
Psychiatry. 2000;48:11051108.
60. Farrer C, Franck N. Sense of body in schizophrenia. Ence-
phale. In press.
61. Priebe S, Rohricht F. Specific body image pathology in acute
schizophrenia patients. Psychiatry Res. 2001;101:289301.
62. Danckert J, Saoud M, Maruff P. Attention, motor control
and motor imagery in schizophrenia: implication for the
role of the parietal cortex. Schizophr Res. 2004;70:241261.
63. Maruff P, Wilson P, Currie J. Abnormalities of motor
imagery associated with somatic passivity phenomena in
schizophrenia. Schizophr Res. 2003;60:229238.
64. Waters F, Jablensky A. Timing judgment deficits in schizo-
phrenia patients with first-rank (passivity) symptoms. Psychi-
atry Res. In press.
65. Blakemore SJ, Wolpert DM, Frith CD. Abnormalities in the
awareness of action. Trends Cogn Sci. 2002;6:237242.
66. Aarts H, Custers R, Wegner DM. On the inference of per-
sonal authorship: enhancing experienced agency by priming
effect information. Conscious Cogn. 2005;14:439458.
67. Repp B, Knoblich G. Toward a psychophysics of agency:
detecting gain and loss of control over auditory action effects.
J Exp Psychol. 2007;33:469482.
68. Wegner DM. The minds best trick: how we experience
conscious will. Trends Cogn Sci. 2003;7:6569.
69. Wegner DM. Precis of the illusion of conscious will. Behav
Brain Sci. 2004;27:649692.
70. Wegner DM, Sparrow B, Winerman L. Vicarious agency:
experiencing control over the movement of others. J Pers
Soc Psychol. 2004;86:838848.
71. Wing JK, Babor T, Brugha T, et al. SCAN. Schedules for
Clinical Assessment in Neuropsychiatry. Arch Gen Psychia-
try. 1990;47:589593.
517
Schizophrenia and Self-recognition

b
y

g
u
e
s
t

o
n

J
u
l
y

6
,

2
0
1
4
h
t
t
p
:
/
/
s
c
h
i
z
o
p
h
r
e
n
i
a
b
u
l
l
e
t
i
n
.
o
x
f
o
r
d
j
o
u
r
n
a
l
s
.
o
r
g
/
D
o
w
n
l
o
a
d
e
d

f
r
o
m

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