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V. Gallese & F. Ferri-Schizophrenia, bodily selves, and embodied simulation.


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Chapter 19

Schizophrenia, bodily selves,


and embodied simulation
Vittorio Gallese and Francesca Ferri

Introduction
The discovery of mirror neurons (Gallese et  al.  1996; Rizzolatti et  al.  1996) and the
­empirical research generated in the following two decades by their discovery has made
it possible to address basic aspects of intersubjectivity on the basis of well-documented
neurophysiological mechanisms and consider intersubjectivity and social cognition from
a novel perspective that emphasizes the crucial role of the acting body. The discovery of
mirror neurons gave us a new, empirically grounded notion of a constitutive aspect of
intersubjectivity: intercorporeality, that is, the mutual resonance of intentionally mean-
ingful sensorimotor behaviors. The ability to understand others as intentional agents does
not exclusively depend on propositional competence but instead is primarily dependent
on the relational nature of action. According to this hypothesis, it is possible to directly
understand others’ basic actions by means of the motor equivalence between what others
do and what the observer can do.
Intercorporeality thus becomes the primordial source of knowledge that we have of others.
The motor simulation instantiated by neurons endowed with “mirror properties” is probably
the neural correlate of this human faculty, describable in functional terms as an instantiation
of embodied simulation (Gallese 2003a, 2005, 2011; Gallese and Sinigaglia 2011b).
Action, though, constitutes only one dimension of the wealth of experiences involved
in interpersonal relations. Every interpersonal relation enables the possibility of sharing
a multiplicity of states such as, for instance, emotions and sensations. Empirical research
demonstrated that, as originally hypothesized by Goldman and Gallese (2000), the very
same nervous structures involved in the subjective experience of emotions and sensations
are also active when such emotions and sensations are observed in others. A multiplicity
of “mirroring” mechanisms are thus present in our brain. It has been proposed that these
mechanisms, thanks to the “intentional attunement” they generate (Gallese 2006), allow
us to recognize others as our fellows, thus making intersubjective communication and mu-
tual understanding possible. The functional architecture of embodied simulation seems
to constitute a basic characteristic of our brain, making possible our rich and diversified
intersubjective experiences, which provide the basis for our capacity to empathize with
others.

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Introduction 349

Mirror neurons, though, are just one instantiation of the cognitive properties of the cor-
tical motor system. Empirical evidence shows that the same motor circuits that control the
ongoing behavior of individuals within their environment also map distances, locations,
and objects in that very same environment, thus defining and shaping in motor terms their
representational content. The way the visual world is represented by the motor system in-
corporates agents’ idiosyncratic ways of interacting with it. To put it simply, the producer
and repository of representational content is not the brain per se, but the brain–body sys-
tem, by means of its interactions with the world of which it is part (see Gallese 2000, 2009;
Ammaniti and Gallese 2014).
In this chapter, we show how this approach can be fruitfully employed to shed new light
on schizophrenia. We cannot fully understand schizophrenia, wrote Minkowski in his
seminal monograph La Schizophrénie (1927), unless we are able to frame it within a thor-
ough account of the structure of subjectivity. Autism, the incapacity to be attuned with the
world, according to Minkowski (1927), therefore constitutes the basic clinical essence of
schizophrenia. Minkowski’s view was derived from insight provided by his mentor Bleuler
(1911), who wrote that schizophrenics cut themselves off from any contact with the exter-
nal world. The core problem of schizophrenics is, accordingly, their lack of “vital contact
with reality” (Minkowski 1927) and can be viewed as an incapacity to “resonate with the
world,” that is, to establish meaningful bonds with other individuals. Contact with reality
is loosened or completely lost not only with respect to transactions with the social world
but also from the first-person perspective point of view.
Phenomenology-inspired psychiatry has generally considered schizophrenia in terms
of this “lack of resonance,” that is, as an empathic disorder. Blankenburg (1971) charac-
terized the autistic dimension of schizophrenia as a global crisis of “common sense,” an
incapacity to pre-reflexively grasp the meaning of the world—a world which looks ter-
ribly unfamiliar and strange to the schizophrenic’s eyes. Parnas and Bovet (1991) linked
the supposed lack of resonance to self-disorder: they argued that schizophrenic autism
derives from a transformation of the structure of subjectivity in its tripartite dimensions:
self-awareness, intentionality, and intersubjectivity. A lack of attunement would, in turn,
be at the origin of the incapacity of schizophrenics to draw a coherent and meaningful
picture of their social world. Parnas et al. (2002) argued that, in schizophrenics, “ex-
perience is more observed than lived,” most likely because of their incapacity to attain a
“non-reflective, tacit sensibility, procuring a background texture or organization to the
field of experience.”
A similar perspective was proposed by Gallese (2003b), who argued that schizophrenic
individuals might suffer problems at the level of pre-reflexive, nonpropositional under-
standing of the world of interpersonal relations, thus showing a defective “shared manifold
of intersubjectivity” (Gallese 2001). Along a similar vein, Stanghellini (2000) argued that
the interpersonal disorders observed in schizophrenic patients constitute a fundamental
aspect of their psychosis. “Defective attunement,” that is, the incapacity to engage oneself
in meaningful relations with others or establish precognitive, noninferential, “intuitive”
interpersonal bonds, would thus represent a major feature of schizophrenia.

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350 Schizophrenia, bodily selves, and embodied simulation

It should be added that this perspective at present does not constitute the mainstream
theoretical approach to schizophrenia, nor does it inspires basic or clinical research into
schizophrenia. However, as recently pointed out by Sass et al. (2011), there is a growing
disillusionment within mainstream psychiatry with the extreme emphasis on operational-
izable concepts introduced in 1982 with the advent of the third edition of Diagnostic and
Statistical Manual of Mental Disorders. As the authors write,
a number of recent editorials by key figures in North American and European psychiatry have noted
the relative lack of real scientific progress in the study of schizophrenia and many other disorders,
and have related this to the loss of validity that can occur when there is an over-focus on reliability
(operational concepts). These editorials have related this lack of progress to the loss, which they la-
ment, of the rich, psychopathological tradition of European psychiatry, which is strongly (but not
exclusively) rooted in phenomenology.
(Sass et al. 2011, p. 2)

In spite of the historically consolidated psychopathological perspective, neuroscientific


research applied to schizophrenia has so far almost entirely neglected the first-person
­experiential dimension of this syndrome, mainly focusing on higher-order cognitive func-
tions such as executive function, working memory, theory of mind, and the like. Some au-
thors have hypothesized that schizophrenia might in fact be characterized by a generalized
dysfunction across all higher-order cognitive functions (Dickinson and Harvey 2009). In
sharp contrast with this view, Sass (2014) pointed out that, although it is true that schizo-
phrenic patients suffer cognitive deficits, such deficits are poorly correlated with clinical
symptoms and lack clinical specificity, as they occur in other psychiatric diseases as well.
We believe that a theoretical approach that views schizophrenia as a self-disorder char-
acterized by anomalous self-experience and awareness may not only shed new light on the
psychopathological features of psychosis but also inspire empirical research targeting the
bodily and neurobiological changes underpinning this disorder.
This perspective is very much consistent with the model of embodied simulation, accord-
ing to which basic forms of intersubjectivity are bodily grounded and rely on neural reuse
(see Gallese 2014). Today cognitive neuroscience can shed new light on self-disorders and
the social deficits characterizing schizophrenia by applying cognitive methods of investiga-
tion to a minimal concept of the self: the “bodily self.” In this chapter, we summarize recent
empirical evidence on the neurobiological basis of the bodily self. We highlight the rela-
tionship between the body, its motor potentialities, and the minimal self. We then compare
our approach with other views on the neural correlates of self-disorders in schizophrenia.
Finally, we propose that cognitive neuroscience can address classic topics of psychopath-
ology by adding a new level of description that enables a correlation to be made between
the first-person experiential aspects of schizophrenia and their neurobiological roots.

The bodily self


The notion of  “self ” is complex and multifaceted. The concept of the minimal, pre-­reflective,
or “core self ” (Rochat 2004) has been extensively debated in cognitive neuroscience,

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The bodily self 351

developmental psychology, and philosophy of mind. Which empirical features such a min-
imal self should possess and what kinds of experience shape it, though, is far from clear.
It is worth emphasizing that the definition of the self at the minimalist level of subjective
experience highlights the potential contribution of bodily experience to its constitution.
Some aspects of the minimal self proposed by contemporary philosophical and empirical
research are the concepts of perspective and first-person perspective, the “mineness” of
the phenomenal field, the question of transparency, embodiment of point of view, and
the issues of agency and ownership (see Cermolacce et al. 2007). On the theoretical side,
phenomenology emphasizes the necessity of embodiment of the self for all the above-cited
aspects of self-experience. As argued by Cermolacce et al. (2007),
[in phenomenology] the field of experience is not yet considered to be subjective because this predi-
cate already implies that there is a subject. For phenomenology, the very idea of the subject ar-
ticulates itself in experience. In this sense, the manifestation and appearing of experience are the
conditions for the experience of the subject in question.

Cermolacce et al. (2007, p. 704)

This philosophical perspective has important implications for empirical studies,


e­specially for those investigating the neural correlates of self-consciousness or self-­
representations. Rather than searching for the neural correlates of a predefined, explicit,
and reflective self-knowledge, the first aim of empirical research should be to investigate
which kind of experience allows an implicit and pre-reflective self-knowledge to emerge,
and how. We thus consider the following questions to be of interest: “What is the basic ex-
perience of ourselves as bodily selves? What enables us to implicitly distinguish ourselves,
as bodily selves, from other human bodies? Could these questions inform the empirical
research agenda applied to psychiatric diseases and, more specifically, to schizophrenia?”
We propose that addressing such questions would make it possible to address core psy-
chopathological aspects of schizophrenia by relating crucial experiential aspects of this
pathology with their bodily and neurobiological bases.
Let’s first highlight the relationship between the body, its motor potentialities, and the
concept of the minimal self. Contemporary research into the minimal self has mostly
focused on body ownership, sense of agency, and first-person perspective. Body owner-
ship refers to “‘the perceptual status of one’s own body, which makes bodily sensations
seem unique to oneself ’” (Tsakiris et al. 2007). Studies on the rubber-hand illusion (RHI;
Botvinick and Cohen 1998) have indicated that multisensory integration is the crucial
mechanism leading to the experience of our body as our own. The RHI is an illusion
that can occur when an individual watches a rubber hand being stroked while his/her
own unseen hand is also being stroked. If the stroking of the rubber and the real hands
occurs synchronously, the position sense of the real hand shifts toward the location of
the dummy hand, and participants feel the dummy hand to be part of their body. How-
ever, as it has recently been argued (see Gallese and Sinigaglia 2010, 2011a), empirical
evidence shows that the multisensory integration leading to the experience of our body
as our own is not the outcome of a mere visual–proprioceptive perceptual association

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352 Schizophrenia, bodily selves, and embodied simulation

(Costantini and Haggard 2007) but is rather conditioned by the possibility—or the lack
thereof—of performing actions with a given body part (Tsakiris and Haggard 2005; Tsa-
kiris et al. 2006, 2007).
The second idea related to the minimal self, sense of agency, refers to the sense of being
the one who generates an action. We recognize ourselves as agents because of the congru-
ence between self-generated movements and their expected consequences. This dominant
role of action over other possible cues for self-identification is accounted for by the central
monitoring theory of action recognition (Frith and Done 1989; Blakemore et al. 2002).
According to the central monitoring theory, each time the motor centers generate an out-
put signal for producing a movement, a copy of this command (the “efference copy”; Holst
and Mittelstedt 1950) is retained and then compared with re-afferent signals (e.g., visual,
kinesthetic) generated by the movement. The predictive component of the model, that is,
the anticipation of the sensory consequences of the movement, is such that, in the case
of a self-produced movement, the actual sensory feedback should match the prediction;
otherwise, sensory signals will be referred to an external event.
However, the central monitoring theory cannot explain the fact that sense of agency
also arises in many situations where action representation is formed but no movement is
executed (see Jeannerod 2007). Because circumstances where actions remain covert are
frequent in our daily life, the existence of an overt behavior should not be a prerequisite
for self-identification. Such circumstances occur, for example, in the case of mental motor
­imagery (Jeannerod 1995) or during the observation of others’ actions, as epitomized by
the mirror mechanism (Gallese 2000, 2006, 2009; Gallese and Sinigaglia 2011b). Starting
from the concept of “shared representations” (see Georgieff and Jeannerod 1998; Gallese
2001), Jeannerod (2007) proposed the model of self–other differentiation as a rotate–­
simulate model.
Finally, the third concept related to the minimal self, first-person perspective, is related
to the phenomenological idea that the world appears to be constrained by a mobile bodily
self, that is, by the spatially located point of view, the orientation, and the attitudes relative
to the subject’s sensorimotor background capacities (Gallese 2000; Cermolacce et al. 2007).
This brief overview shows that the concepts adopted by contemporary r­ esearch to define
the minimal self as a bodily self often refer to the motor system.
More radically, it has been recently proposed (Gallese and Sinigaglia 2010, 2011a) that
there is a sense of body that is enactive in nature and enables the formation of the most
primitive concept of the self, the bodily self. According to this perspective, the body acts
primarily as a source of power for action (Gallese and Sinigaglia 2010). The minimal con-
cept of the self, the bodily self, tacitly presupposes ownership of an action-capable agent-
ive entity. Hence, this primitive sense of the self primarily rests on the workings of the
motor system. Our body is experienced as the set of all the motor potentialities that define
the horizon of our interaction with the world. This is what Straus’s (1960) concept of the
human structural plan (Bauplan) refers to. Such a primitive sense of the self as a self-
propelled, mobile, bodily self is thought to be antecedent to the distinction between sense
of agency and sense of ownership.

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The bodily self 353

How does such a notion of the bodily self relate to the brain? Neuropsychological and
neuroimaging studies have demonstrated that the body is a “unique” object: specific brain
structures are involved in the visual processing of the human body (Downing et al. 2001;
Peelen and Downing 2007; Moro et al. 2008). Viewing nonfacial body parts selectively
­activates the lateral occipitotemporal cortex (OTC), in an area called the extrastriate body
area (EBA), and an area located in the fusiform gyrus, the fusiform body area (Schwarzlose
et al. 2005; Peelen and Downing 2007). Moreover, there is a topographically organized
body part map in the OTC: a recent study has demonstrated the presence of a hand-­
selective region in the left lateral occipital sulcus, in an area that partially overlaps with the
EBA, although the authors of this study suggested that this region could be functionally
and anatomically dissociated from the EBA (Bracci et al. 2010).
However, self-body recognition requires more than a mere visual pictorial representa-
tion. When observing a human body, we also do something very different from what we
do when we look at inanimate objects or at other nonhuman living creatures: we must
distinguish our own body from the body of others. Studies using different methods (i.e.,
behavioral methods, functional MRI [fMRI], and transcranial magnetic stimulation) have
shown that recognition of one’s own body is independent from the recognition of other
people’s bodies (Sugiura et  al.  2006; Devue et  al.  2007). Interestingly, self-related body
stimuli are processed faster and more accurately than other-related body stimuli are. This
effect has been termed “self-advantage” (see Frassinetti et al. 2008, 2009).
The relationships between the minimal sense of self, self-body recognition, and the cortical
motor system have recently been demonstrated. Ferri et al. (2011) showed that the motor
experience of one’s own body, even at a covert level, allows an implicit and pre-reflective
bodily self-knowledge to emerge, leading to a self–other distinction. Participants’ responses
during a hand mental rotation task respond more quickly to pictures of their dominant hand
than to pictures of others’ hands (Ferri et al. 2011). The same study also showed that, when
participants were requested to explicitly discriminate between their hands and the hands
of others, the self-advantage disappeared. Implicit and explicit recognition of the bodily
self dissociated: only implicit recognition of the bodily self facilitated implicit bodily self-­
processing. The authors of this study hypothesized that the implicit self-advantage could be
due to the stronger motor simulation induced by the observation of one’s own hand.
A subsequent fMRI study by Ferri, Frassinetti, Ardizzi, et al. (2012), who used a simi-
lar hand mental rotation task, corroborated this hypothesis by revealing how implicit
self-advantage correlates with strong activation of the cortical motor system. The results
demonstrated that the contralateral ventral premotor cortex was uniquely and specifically
activated during the mental rotation of the participants’ own dominant hands. Further-
more, this mental process activated a bilateral cortical network formed by supplementary
and presupplementary motor areas, the anterior insula and the occipital cortex.
The ventral premotor cortex is an essential anatomofunctional base for the motor aspect
of bodily selfhood, given its role in integrating self-related multisensory information. In-
deed, clinical and functional evidence indicates the systematic involvement of the ventral
premotor cortex in body awareness (Berti et al. 2005; Arzy et al. 2006). There is a close

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354 Schizophrenia, bodily selves, and embodied simulation

relationship between the bodily self-related multimodal integration carried out by the cor-
tical motor areas, which specify the motor potentialities of one’s body and guide motor
behavior, and the implicit awareness one entertains of one’s body as one’s own body and of
one’s behavior as one’s own behavior.
The ventral premotor cortex is perfectly suited for this job, because it is anatomically
connected both to visual and somatosensory areas in the posterior parietal cortex and to
frontal motor areas. Activity in the ventral premotor cortex likely integrates multisensory
signals from one’s own body parts and maps them onto the motor schemata that, in turn,
guide possible movements and actions. Such mapping is constrained by the motor poten-
tialities of those very same body parts.
The motor aspects of the bodily self enable the integration of self-related multimodal
sensory information both about the body and about the world the body interacts with.
Thus, the body part–related multimodal integration mechanism in the ventral premotor
cortex could be—at least partly—responsible for the feeling of body ownership. This no-
tion of the minimal self as the bodily self is important also from a theoretical point of view,
because it opens up the possibility of linking the openness of the self to the world via the
motor potentialities the bodily nature of the self entails.
In the next section, we show how such multimodal integration appear to be deficient in
schizophrenia, and how such deficiency could lead to both self-disorders and social deficits.

The loss of implicit self-knowledge and self–other


differentiation: schizophrenia and the bodily self
The term “schizophrenia spectrum” is used to describe a category of disorders affecting
the functioning of the minimal or “core” self (Zahavi 2005), which is also referred to as
“ipseity” (Parnas 2000; Sass and Parnas 2003, 2007). Self-disorder (Nelson et al. 2008) is
a concept whose complexity seems to reflect the multilayered concept of self-experience.
Disorders of self-experience are evident in the prodromal phase of schizophrenia and are
closely interrelated with the subsequent development of the disease (Parnas 2003).
The term “self-disorder” in schizophrenia refers to a state in which the minimal self is
fragile, unstable, and affected in at least three basic phenomenological aspects: (1) phe-
nomenality (appearing); (2) first-person perspective; and (3) self-presence (Cermolacce
et al. 2007). In line with this account, “self-disorder” in schizophrenia has elsewhere been
described as a disembodiment of the self (Fuchs 2005; Stanghellini 2009). As argued by
Fuchs (2005), schizophrenic patients do not inhabit their body, in the sense of using the
body as a medium for relating to the world.
At a more general level, the phenomenological approach to schizophrenia proposes the no-
tion of embodiment as central to understanding different symptoms such as loss of self and
loss of common sense, as well as intentionality disorders. According to this approach, the
coherence between these heterogeneous symptoms can be detected when their associations
with the body are revealed: that is, the loss of the ability to function normally within one’s body
leads to an inability to interrelate with others (Fuchs 2005; Stanghellini and Ballerini 2011).

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The loss of implicit self-knowledge and self–other differentiation 355

In a clinical case reported by Fuchs (2005), a young schizophrenic patient described how
she underwent a progressive alienation from her bodily feelings and had increasing diffi-
culty in recognizing the way she moved or behaved:
For some time I had a feeling as if my clothes did not seem appropriate any more. My gait had
changed, I walked stiffly and did not know how to hold my hands. Then I often looked into the mir-
ror and found that my facial expression had changed, and I began to think that I might be regarded
as a prostitute. Men looked so strange at me . . . I took passport pictures of myself in order to examine
whether I only imagined that. Then I began to feel a kind of charging or tension in my body when
others came near to me, as if it were passing over from them. Finally I thought I should be made a
prostitute by brain manipulation.
(Fuchs 2005, pp. 103–4)

The sense of disembodiment experienced by the patient led her to use a delusional
explanation (i.e., that others were manipulating her brain) to rationalize her state. This
example illustrates that one of the first signs of schizophrenia is the disturbance of the
bodily self. Congruently, two of our recent studies have demonstrated that implicit know-
ledge about the bodily self is impaired and that self–other discrimination is problematic
in first-episode schizophrenia patients. In the first study, implicit and explicit knowledge
of the bodily self was assessed in two separate experiments carried out on healthy volun-
teers (Frassinetti et al. 2011). Both experiments used body effectors (hands and feet) or
inanimate objects (shoes and mobile phones) as stimuli. In the first experiment, which as-
sessed implicit knowledge, participants had to decide which of two images of body parts
or inanimate objects matched a target image portraying the same body part or object. In
the second experiment, which assessed explicit knowledge, they had to determine which
of the two images was of a body part or inanimate object that belonged to them. In both
experiments, half of the images portrayed patients’ own body parts or inanimate objects,
and the remaining half portrayed strangers’ body parts or inanimate objects.
The results showed that healthy participants were more accurate in the implicit task
when the images portrayed were of their own body parts than when the images were of
the stranger’s body parts, that is, they exhibited self-advantage. In contrast, self-advantage
was not found when explicit recognition of one’s own body parts was required. Moreover,
self-advantage was also not observed when the images were of inanimate objects, in either
the implicit task or the explicit task.
The second study demonstrated that first-episode schizophrenic patients, unlike healthy
controls, did not show self-advantage when viewing body parts in the implicit task (Ferri,
Frassinetti, Mastrangelo, et al. 2012). In contrast, the patients’ performance when inani-
mate objects were shown did not differ from that of the healthy participants. Furthermore,
when required to recognize their own body parts, patients made a higher percentage of
self-misattribution errors than control participants did. These results show that first-­
episode schizophrenic patients suffer from a disturbed implicit sense of their bodily self.
One could argue that our results could be biased due to the presence of general alterations
in higher cognitive functions—for example, working memory—as they are frequently
found in schizophrenia. However, we believe such alterations were not responsible for the

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356 Schizophrenia, bodily selves, and embodied simulation

lack of self-advantage, for the following reasons: first, patients’ accuracy with inanimate ob-
jects did not differ from that seen with healthy participants, an observation that excludes
the possibility that the patients had a general inability to perform the task; second, previ-
ous studies investigating sense of agency and body ownership in schizophrenia (Daprati
et al. 1997; Peled et al. 2000; Thakkar et al. 2011) similarly showed a specific lack of bodily
self-knowledge, thus supporting our hypothesis that there is a specific alteration of bodily
self-consciousness in schizophrenia.
Our study, however, provides additional insight, as it demonstrates that self–other dis-
crimination impairments in schizophrenia are already present at the very basic level of
the implicit processing of body stimuli. When required to determine which of two images
showed their own body part, schizophrenic patients failed to distinguish between images
of their own body parts and those of other people’s body parts, that is, they tended to mis-
attribute other people’s body parts to themselves. On the basis of what we showed in sec-
tion “The bodily self,” it can be hypothesized that the lack of self-advantage in first-episode
schizophrenic patients may be due to a disruption of their awareness of the bodily self.
Further proof of the close relationships between self-disturbance, a defective sense of
bodily self, and social impairments comes from a functional MRI (fMRI) study on so-
cial perception of touch (Ebisch et al. 2012). Twenty-four first-episode schizophrenic pa-
tients and 22 healthy control participants underwent fMRI during a social perception task,
which required them to watch videos depicting individuals being touched by an inani-
mate object or by another individual, and a tactile localizer condition, in which partici-
pants’ hands were touched. Activation in the ventral premotor cortex in response to the
observation of bodily tactile stimulations was reduced in the schizophrenic group and
negatively correlated with self-experience disturbances, as assessed with the Bonn Scale of
Basic Symptoms.1 As we argued before, the ventral premotor cortex may be a key structure
underlying the breakdown of self-monitoring. Such a breakdown could then lead to the
blurring of self-boundaries and, consequently, to confusion regarding the interrelation-
ship of the self with others.
A second interesting result from this study was the absence of blood oxygenation
level–dependent suppression in the posterior insular cortex in schizophrenic patients
when they observed another individual being touched. Deactivation in the posterior in-
sular cortex in the healthy control group has previously been shown to be a response that
is specific for the observation of social affective touch (Ebisch et al. 2011). Accordingly,
we found that levels of activation in the posterior insular cortex in the healthy control

1 Basic symptoms describe anomalous self-experiences representing subjective, subclinical, experiential


disturbances in the domains of cognition, perception, bodily experience, action, and emotion (Huber
1983; Klosterkotter 1992). To some extent, basic symptoms overlap with self-disturbances conceived
as trait phenomena identified via the Examination of Anomalous Self-Experience symptom checklist
(Parnas et al. 2005). Basic symptoms reflect the initial experiential changes that set off the development
of schizophrenic psychotic symptoms, and such symptoms have been reported to occur in all stages of
the disease.

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The loss of implicit self-knowledge and self–other differentiation 357

group were significantly different from those in schizophrenic patients, specifically in


response to the observation of social affective touch carrying either a positive or a nega-
tive valence (i.e., a caress or a slap). In addition to its role in social perception (Ebisch
et al. 2011), the posterior insular cortex is considered to be critical for interoception,
as well as being a central node of the system that provides the neural representation of
“the material me” (Craig 2002). Accordingly, there is plenty of empirical evidence sug-
gesting that the posterior insular cortex may be involved in self-awareness (Botvinick
and Cohen 1998; Tsakiris et al. 2007), body part awareness (Karnath et al. 2005), and
the sense of agency (Farrer et al. 2003). Hence, given the role of the posterior insular
cortex in interoception and bodily self-awareness (Craig 2002; Botvinick and Cohen
1998; Tsakiris et al. 2007; Karnath et al. 2005; Farrer et al. 2003), we propose that the
absence of its deactivation in first-episode schizophrenic patients during the observa-
tion of another individual experiencing social affective touch may reflect a deficit in
the pre-reflective suppression of self-oriented affective arousal, suppression which likely
normally contributes to the differentiation between self and other. Disturbances of bod-
ily self-­experience may thus have a primary role in schizophrenia and may—at least
partly—account for the social deficits observed in schizophrenic patients.
Further evidence relating altered self-experience with defects in the multisensory inte-
gration carried out by the ventral premotor cortex comes from two recent studies where
we investigated the sense of body ownership in schizophrenic patients. In the first study
(Ferri, Chiarelli, et al. 2013), which was carried out on healthy volunteers, the participant
was seated so that his/her right arm rested upon a small table just below another table;
thus, the participant’s hand was hidden from view. Then, a life-sized rubber model of a
right hand was placed on the table in front of participants. Participants observed the ex-
perimenter’s hand approach—but not touch—the rubber hand. The phenomenology of the
illusion was assessed via a questionnaire and by measuring the skin conductance response.
Both measures indicated that participants experienced the illusion that the e­ xperimenter’s
hand was about to touch their hidden hand rather than the rubber hand, as if the latter had
replaced their own hand. This did not occur when the rubber hand was rotated by 180° or
was replaced by a piece of wood.
This illusion indicates that our brain does not build a sense of bodily self in a merely pas-
sive and reactive way, via perceptual correlations; rather it generates predictions based on
what may or may not belong to itself. Since embodiment of the rubber hand only occurred
when the approaching experimenter’s hand entered participants’ peripersonal space, we
hypothesize that this illusion requires the recruitment of the ventral premotor cortex,
where body-related sensory information (i.e., tactile, visual, and auditory) is integrated by
neurons that both map the motor potentialities and control the actual movements of body
parts (Bremmer et al. 2001); specifically, that it requires the recruitment of the human
homolog of the macaque monkey area F4 (Fogassi et al. 1996; Rizzolatti et al. 1997).
When submitted to the same experimental protocol, schizophrenic patients showed a
weaker sense of ownership over the rubber hand than healthy controls did (Ferri, Costan-
tini, et al. 2013). Furthermore, susceptibility to the RHI correlated with negative symptoms:

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358 Schizophrenia, bodily selves, and embodied simulation

the self-reported strength of the illusion was related to an increased score on the anhedo-
nia subscale of the Scale for the Assessment of Negative Symptoms. ­Anhedonia—the in-
ability to experience pleasure—is a symptom of several psychiatric disorders. However,
authors in the tradition of phenomenological psychiatry considered it to be a fundamental
manifestation of self-disorder in schizophrenia (see Sass and Parnas 2003). These authors
argued that anhedonia might be viewed as the outcome of a more profound alteration of
self-experience in schizophrenia, that is, the disturbance of sense of self, or ipseity. Thus,
anhedonia would not be an independent dysfunction. Indeed, according to Sass and Par-
nas (2003), ipseity is a necessary condition for the experience of many forms of pleasure.
Interestingly, one aspect of ipseity, other aspects of which include corporeality, stream of
consciousness, self-demarcation, and existential orientation, is the mineness of experience
(Parnas and Sass 2001; Parnas and Handest 2003). In summary, the negative symptom an-
hedonia may reflect a basic alteration of the mineness of experience and, as such, would
positively correlate with patients’ ownership of the rubber hand.
As mentioned in section “The bodily self,” the human ventral premotor cortex is activated
during the implicit processing of one’s own hand (Ferri, Frassinetti, Ardizzi, et al. 2012).
Given that the ventral premotor cortex appears to be hypofunctional in schizophrenia,
as well as negatively correlated with self-experience disturbances (Ebisch et  al.  2012),
and since it has been demonstrated that schizophrenic patients show a defective impli-
cit sense of their bodily self (Ferri, Frassinetti, Mastrangelo, et al. 2012), we hypothesize
that ­patients’ defective anticipatory sensorimotor processing of touch might have the same
premotor origin (see also Gallese and Ferri 2013). All these results point to the existence
of a close relationship between the bodily self-related multimodal integration carried out
by the cortical motor areas, which both specify the motor potentialities of one’s body and
guide its motor behavior, and the implicit awareness one entertains of one’s body as one’s
own body and of one’s behavior as one’s own behavior. Altered functionality of these brain
networks therefore appears to be linked to self-disorders in schizophrenic patients.

Schizophrenia, the self, and brain midline regions


The literature reviewed so far clearly supports the hypothesis that abnormalities of self-
experience represent elementary features of schizophrenia. We have particularly focused
on the empirical evidence of abnormalities of bodily self-consciousness in schizophrenia,
such as the loss of the implicit recognition of self-body parts, the explicit self-misattribution
of the same body parts when belonging to others, and the blurring of peripersonal space
boundaries as well as of self–other boundaries. In addition, we have discussed the associ-
ation of these symptoms with dysfunctions of brain lateral cortices (i.e., the ventral pre-
motor cortex and the insula). However, it should be added that another perspective on
self-disorders in schizophrenia has been proposed; this perspective views these disorders as
being caused by dysfunction of brain midline regions involved in self-referential processes
(Northoff et al. 2006; Qin and Northoff 2011) and the default mode network (DMN; see
Raichle et al. 2001).

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Conclusions 359

From this perspective, schizophrenia is associated with changes in the functional con-
nectivity (Whitfield-Gabrieli et  al.  2009) and homogeneity of the midline cortex (Guo
et al. 2014), an anterior-to-posterior shift during self-reflection (Holt et al. 2011), as well
as with aberrant coupling within and across the DMN and other brain networks (Wotruba
et al. 2013). Moreover, the posterior cingulate cortex (PCC), which is a crucial node in
the DMN (Buckner et  al.  2008), is commonly implicated in schizophrenia (Northoff
et al. 2005; Skudlarski et al. 2010).
Recent studies suggest that these two perspectives on self-disorders in schizophrenia—the
one linking them to dysfunction in the lateral cortex (i.e., the ventral premotor cortex and
the insula), and the other associating them with alterations in midline brain structures—are
intimately interrelated (Ebisch et al. 2013). As we argued above, the ventral premotor cortex
and the posterior insular cortex (pIC) may be involved in disturbances in self-experience and
self–other relationship. Results from functional interaction analysis in first-episode schizo-
phrenia patients, as compared to healthy controls, showed aberrant functional interactions
of the right ventral premotor cortex and the bilateral pIC with the PCC (Ebisch et al. 2013).
More specifically, increased functional coupling between the ventral premotor cortex and
the PCC was found to positively correlate with basic symptoms (subjective self-experience
disturbances). Moreover, the pIC showed reduced functional coupling with the PCC and
the postcentral gyrus, and increased functional interactions with the anterior insula.
Altogether, these data suggest that altered functional interactions involving the pIC and
the ventral premotor cortex converge on the PCC. Ebisch et al. (2013) interpreted these re-
sults as indicating an imbalance between processing internally guided information (which
occurs in the pIC) and processing externally guided information (which occurs in the
ventral premotor cortex) and a consequent abnormal integration of these two types of in-
formation with self-referential processing, which is mediated by the PCC. The PCC is part
of an anatomical and functional unit that comprises various medial cortical regions, such
as the medial orbital prefrontal cortex, the ventromedial prefrontal cortex, the sub/pre-
and supragenual anterior cingulate cortex, the dorsomedial prefrontal cortex, the medial
parietal cortex, and the retrosplenial cortex. Recently, these regions have been subsumed
under the term “cortical midline structures” and associated with self-referential process-
ing per se (Northoff and Bermpohl 2004; Gillihan and Farah 2005; Northoff et al. 2006).
On the basis of these results, we hypothesize that, in schizophrenia, the complexity of
the multifaceted self-disorders, including altered bodily self-consciousness, likely relies
on an imbalance in the functioning of and relationship between different brain networks,
where midline structures may play a mediating role. Further studies will be necessary to
empirically test and, hopefully, eventually confirm our hypothesis.

Conclusions
The Italian psychopathologist Arnaldo Ballerini (2012), echoing the words of Blank-
enburg (1971), argued that the time has come to address schizophrenia as originating
from the “transcendental deficit” seen in schizophrenic patients, that is, their inability

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360 Schizophrenia, bodily selves, and embodied simulation

to simultaneously constitute the self and its relationship with the world. This appears to
be the fundamental ontological deficit from which the main ontic aspects of the disease,
such as negative and positive symptoms, derive. The constitution of the self is intrinsically
­related to the constitution of the other as a self. This starting point is highly consistent with
the reciprocity linking self and other, as conceived by the model of embodied simulation
(Gallese 2014).
As argued elsewhere (Gallese and Ferri 2013), we believe that the potentiality for action
our bodies normally instantiate might provide the core nucleus that gives rise to the bodily
presence that characterizes a competent self–other relationship. The enigmatic nature of
the world, particularly the world of others, makes it almost impossible for schizophrenic
patients to interpret it correctly, given their defective bodily presence. We hypothesize that
the empirical findings here reviewed represent preliminary evidence of the neural mech-
anisms underpinning defective forms of bodily presence in schizophrenia.
It has been proposed that social dysfunction in schizophrenic patients primarily arises
from disturbances of bodily self-experience (Parnas et al. 2002; Gallese 2003b; Sass and
Parnas 2003) rather than from disturbances of the intersubjective domain. It should be
added, though, that the debated primacy either of the self or intersubjectivity in social
cognition is probably a sort of chicken–egg question. A distinctive feature of mammals in
general, and of primates in particular, is that they are born inside the other and with the
other. The concepts of “self ” and “other” are mutually dependent: there is no self without
the other, and vice versa. Self and other are linked by means of the relational character of
the human condition. Therefore, it is probably a useless exercise, as Ballerini (2012, p. 142)
argues, to try to determine whether self-constitution or other-constitution plays a primary
causal role in the making of the natural evidence of the world, as both are closely and inex-
tricably intertwined (see also Ammaniti and Gallese 2014; Gallese 2014).

Acknowledgments
This work was supported by an EU “Towards an Embodied Science of InterSubjectivity”
grant (TESIS, FP7-PEOPLE-2010-ITN, 264828) to V. G.

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