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Brain and Cognition 90 (2014) 8799

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Brain and Cognition


journal homepage: www.elsevier.com/locate/b&c

Disturbances of spontaneous empathic processing relate with the


severity of the negative symptoms in patients with schizophrenia:
A behavioural pilot-study using virtual reality technology
Brangre Thirioux a,,1, Louis Tandonnet b,2, Nematollah Jaafari b,c,d,e,f, Alain Berthoz a
a
Laboratoire de Physiologie de la Perception et de lAction, CNRS UMR 7152, Collge de France, 11 Place Marcelin Berthelot, Paris F-75005, France
b
CIC INSERM U 802, CHU de Poitiers, Poitiers F-86022, France
c
INSERM U 1084, Experimental and Clinical Neurosciences Laboratory, Poitiers F-86022, France
d
Universit de Poitiers, Facult de Mdecine, Poitiers F-86022, France
e
Unit de Recherche Clinique intersectorielle en psychiatrie vocation rgionale (URC) du Centre Hospitalier Henri Laborit, Poitiers F-86022, France
f
Groupement de Recherche, CNRS 3557, France

a r t i c l e i n f o a b s t r a c t

Article history: Behavioural and neuroimaging data have recently pointed out that empathy (feeling into someone else) is
Accepted 9 June 2014 associated with mental imagery and transformation related to ones and others visuo-spatial perspectives.
Available online 9 July 2014 Impairments of both empathic and visuo-spatial abilities have been observed in patients with schizophre-
nia. Especially, it has been suggested that schizophrenics are altered in spontaneously simulating another
Keywords: individuals rst-person experience. However, there is so far only little evidence regarding the relationship
Schizophrenia between decits in empathy and disturbances in spontaneous heterocentered coding in schizophrenia. In
Empathy
the present pilot-study, we tested with schizophrenic patients our behavioural paradigm that enables to
Sympathy
Negative symptoms
measure from the bodily postures and movements whether individuals in ecologically more valid condi-
Executive functions tions are interacting with another individual by using egocentered as in sympathy (feeling with someone
Inhibitory processing else) or heterocentered as in empathy visuo-spatial mechanisms. For that, ten patients and ten con-
trols, standing and moving, interacted with a virtual tightrope walker, displayed life-sized, standing and
moving as well. We show that patients with higher negative symptoms had, in most cases, decits in spon-
taneously using heterocentered visuo-spatial mechanisms and employed preferentially an egocentered
referencing to interact with the avatar. In contrast, preserved spontaneous heterocentered visuo-spatial
strategies were not linked to a prevailing negative or positive symptomatology. Our data suggest that
the severity of the negative symptoms in schizophrenia relates with disturbances of spontaneous (on-
line) empathic processing in association with lower scoring self-reported trait cognitive empathy.
2014 Elsevier Inc. All rights reserved.

1. Introduction Shur, Harari, & Levkovitz, 2007; Sperber & Wilson, 2002). Under-
standing the structure of these social behavioural impairments is
Clinical data from behavioural and neuroimaging studies with of critical importance for establishing predictive markers of the ill-
psychiatric populations have provided increasing support that ness as social abnormalities have been often observed to precede
schizophrenia is associated with deviant social functioning (Brne, the psychosis outcome (Brne, 2005b; Schenkel, Spaulding, &
2005a; Corrigan & Nelson, 1998; Frith, 2004; Shamay-Tsoory, Silverstein, 2005). Notably, schizophrenic patients and people with
high schizophrenia-like traits have been suggested to suffer respec-
Corresponding author. Address: Laboratoire de Physiologie de la Perception et tively from altered and reduced empathic abilities (Decety &
de lAction, Collge de France, 11 Place Marcelin Berthelot 75231, Paris cedex 05, Moriguchi, 2007; Dinn, Harris, Aycicegi, Greene, & Andover, 2002;
France. Fax: +33 1 44 27 13 82. Henry, Bailey, & Rendell, 2008; Lee, Farrow, Spence, & Woodruff,
E-mail address: berangerethirioux@hotmail.com (B. Thirioux). 2004; Milgram, 1960; Montag, Heinz, Kunz, & Gallinat, 2007;
1
Present address: Institute for Advanced Studies of Paris, 17 Quai dAnjou, Paris Shamay-Tsoory et al., 2007; Thakkar & Park, 2010). However, there
F-75004, France.
2 is only limited evidence regarding the relation between empathy
Present address: Service universitaire daddictologie de liaison du C.H.U de
Nantes, Nantes F-44093, France. decits and schizophrenia (Bora, Gken, & Veznedaroglu, 2008).

http://dx.doi.org/10.1016/j.bandc.2014.06.006
0278-2626/ 2014 Elsevier Inc. All rights reserved.
88 B. Thirioux et al. / Brain and Cognition 90 (2014) 8799

1.1. The multidimensional approach of empathy second-person signals, moment-to-moment adaptation to changes
in the others behaviours, and maintaining self-other distinction
Empathy is the capacity to share, react to and understand the (Berthoz, 2004; Berthoz & Thirioux, 2010; Thirioux & Berthoz,
lived experience and associated mental state of others (Davis, 2011; Thirioux, 2011).
1980, 1994). As a complex and multifaceted socio-cognitive con- Using electrical neuroimaging (EEG)-based measurements with
struct (Berthoz, 2004; Preston, 2007; Preston & de Waal, 2002; non-clinical populations, we reported that heterocentered coding
Thakkar, Brugger, & Park, 2009), empathy incorporates automatic, in empathy is sustained by activations in the left temporo-parietal
emotional, cognitive and regulatory processes and combines junction (TPJ) at 520630 ms post-stimulus onset (PSO) (Thirioux
cooperating and/or competing activations (Berthoz, 2004) in et al., 2010) and preceded by sequential activations in the mirror
topographically distributed and functionally distinct brain net- neuron system (MNS) from the left insula to the right inferior fron-
works (Decety, 2007; Decety & Jackson, 2004). The automatic tal gyrus (IFG) via the inferior parietal lobule (IPL) at 65425 ms
and emotional components of empathy similar to the rst-person and co-activations in the right dorsolateral prefrontal cortex
like processes involved in simulation (Goldman, 2006) enable to (dlPFC) at 330425 ms (Thirioux et al., 2014). This activation of
internally reproduce another persons subjective experience, as if the TPJ a key-region of the heteromodal cortex and vestibular
individuals were experiencing this given mental state themselves. system integrating body-related and self-location information
The cognitive and regulatory components refer to a controlled (Blanke, Landis, Spinelli, & Seeck, 2004; Blanke, Ortigue, Landis, &
process whereby people understand the mental state of others Seeck, 2002; Kahane, Hoffmann, Minotti, & Berthoz, 2003; Lobel,
while adopting their psychological viewpoint based upon perspec- Kleine, Bihan, Leroy-Willig, & Berthoz, 1998) and sustaining per-
tive-taking and self-other distinction. These are strongly akin to spective-taking in ToM (Decety & Lamm, 2007; Schnell, Bluschke,
the processes involved in Theory of Mind (ToM) (Premack & Konradt, & Walter, 2011) strengthens the hypothesis that
Woodruff, 1978) or mentalizing (Frith & Frith, 2003) which is the empathy is associated with visuo-spatial transformations. More-
ability to represent and attribute mental state to others. Self-regu- over, this earlier recruitment of the executive functions in our data
lation mechanisms further contribute to decoupling computational echoed inhibitory processes and shifts from egocentered strategies
mechanisms between rst- and second-person information and in the MNS to heterocentered strategies in given nodes of the men-
tap into executive functions (Decety & Jackson, 2004; Decety & talizing network (TPJ) (Frith & Frith, 2006) (Thirioux et al., 2014). It
Michalska, 2009; Frith & Frith, 2003; Ochsner & Gross, 2005; Van corroborates the view that non-egocentered simulation requires
der Meer, Groenewold, Nolen, Pijnenborg, & Aleman, 2011). inhibiting ones egocentered perspective (Nardini, Burgess,
Breckenridge, & Atkinson, 2006) and is dlPFC-dependent (Van der
1.2. The visuo-spatial and body-related mechanisms in empathy Meer et al., 2011; Vogeley et al., 2001). In the same vein, a correla-
tion has been found between rightward biases in spatial attention
Although empathy i.e., putting oneself in the others shoes and scores to affective empathy in self-rating questionnaires
is generally admitted to require both self-other distinction and (Thakkar et al., 2009). And, Mohr et al. (2010) reported that faster
psychological perspective-taking, little experimental work has reaction times (RTs) in egocentered transformation tasks positively
focused on self-regulation and more basic visuo-spatial mecha- correlate with high scoring self-reported trait empathy.
nisms (Thakkar & Park, 2010). However, recent studies have shown
that empathy entails mental imagery and transformations related 1.3. Heterocentered vs. egocentered referencing dissociate empathy
to ones and others visuo-spatial perspective (Mohr, Rowe, & from sympathy
Blanke, 2010; Thakkar et al., 2009; Thirioux, Jorland, Bret,
Tramus, & Berthoz, 2009; Thirioux, Mercier, Blanke, & Berthoz, Disentangling the involvement of egocentered vs. heterocen-
2014; Thirioux, Mercier, Jorland, Berthoz, & Blanke, 2010). The pre- tered visuo-spatial mechanisms in empathy is essential as it
requisite for empathy or feeling into (from the Germane ein further enables to dissociate empathy from sympathy or feeling
[into] fhlen [to feel]; Jorland & Thirioux, 2008) is a sort of with (mit [with] fhlen; Jorland & Thirioux, 2008; Hojat et al.,
awareness of being outside the other person and having to reach 2011; Hojat, Spandorfer, Louis, & Gonnella, 2011). These intersub-
[her/him] (Gelhaus, 2011). It enables to understand the others jective phenomena are most often conated in experimental
current experience as the experience of someone else while distin- studies with non-clinical, neurological and psychiatric populations.
guishing oneself from the other (Decety, 2007; Decety & Jackson, This is doubtless due to that empathy and sympathy are closely
2004; Hein & Singer, 2008; Singer et al., 2004). Therefore, empathy related and in part converge. The feeling, common to both phe-
requires perspective-change and is based upon a mental transfor- nomena, corresponds to the mental experience of ones physiolog-
mation of ones own-body in space in which individuals are map- ical and bodily states and changes (Damasio & Carvalho, 2013) that
ping their body into the others body in a rotation-like manner are generated by the perception of the others current experience
[Self ? Other] (Thirioux et al., 2009, 2010). Accordingly, empathy and enables to access the embodied mind of others, i.e., in their
specically modulates self-location (the experience of where I bodily and behavioural expressions (Zahavi, 2008). However,
am in space; Blanke, 2012) and the egocentered (centered on ones when sympathizing (feeling with), individuals are feeling the same
own-body) visuo-spatial perspective (the experience from which I thing as others are feeling (the same kind of inner state; Gelhaus,
perceive the world; Blanke, 2012), two key phenomenological 2011) and at the same time (Olinick, 1987), tending to merge iden-
aspects of the bodily self which are substantial for self-other inter- tities (Wilmer, 1968). It leads to attributing the others experience
action. Empathy is, thus, associated with disembodied self-location to oneself as if individuals were the other person (Gelhaus, 2011).
(in which the imagined self-location does not match the position of This self-attribution is based upon a body-related mental imagery
ones physical body in space; Blanke et al., 2005) and heterocen- and spatial transformation process in which individuals are map-
tered (centered on another individuals body; Cleret de Langavant ping the others body into their own-body in a mirror-like linear
et al., 2011; Degos, Bachoud-Lvi, Ergis, Petrissans, & Cesaro, manner [Other ? Self] (Thirioux et al., 2009, 2010). Accordingly,
1997) visuo-spatial perspective (Fig. 1A). sympathy is associated with embodied self-location (the normal
We have newly assumed that empathy relies upon continual experience that the self is located within ones bodily borders at
and bi-directional perspective-change processes, i.e., dynamic a specic position in space; Arzy, Thut, Mohr, Michel, & Blanke,
shifts between the egocentered and heterocentered visuo-spatial 2006) and egocentered visuo-spatial perspective (Fig. 1A), i.e.,
frameworks, enabling on-line comparisons between rst- and without perspective-change, contrary to empathy (Berthoz &
B. Thirioux et al. / Brain and Cognition 90 (2014) 8799 89

Fig. 1. Theoretical schemas. (A) Empathy (feeling into; left column) and sympathy (feeling with; right column) are associated with distinct self-location (disembodied vs.
embodied) and visuo-spatial mechanisms (heterocentered vs. egocentered) (see the red and blue dotted arrows). (B) Two individuals, A (in red; or Self) and B (in blue; or
Other) are facing each other. In rotation symmetry, reecting empathy (left column), A is leaning to his right when B is leaning to his right (black arrow) and vice versa (i.e.,
leftleft). In reection symmetry, reecting sympathy (right column), A is leaning to his left when B is leaning to his right (black arrow) and vice versa (i.e., rightleft)
(adapted from Thirioux et al., 2009, 2010).

Thirioux, 2010; Thirioux, 2011; Thirioux & Berthoz, 2011). In our perspective-taking transformation tasks have been demonstrated
prior EEG studies, egocentered visuo-spatial mechanisms in sym- to correlate with higher scores to self-reported questionnaire sub-
pathy triggered the typical whole sequence of activations within scales assessing the cognitive components of empathy in schizo-
the MNS (Nishitani & Hari, 2000, 2002), i.e., from the insula and typal women and higher positive schizotypy across genders
superior temporal cortex, via the IPL-IFG, until the output end of (Thakkar & Park, 2010). Landgraf et al. (2010) further reported that
the mirroring processing in the somatosensory and motor cortices computing object-to-object relations (allocentered computation)
from 65 ms to 630 ms PSO (Thirioux et al., 2010, 2014). These trigger increased RTs and errors rates in chronic patients, com-
data suggested that sympathy, in contrast to empathy, was not pared to controls, whereas own-body centered judgments were
associated with inhibitory processes and shift from ego- to preserved. Patients were also found to have decits in shifting from
heterocentered strategies. an egocentered to an allocentered perspective.
However, critical aspects regarding the alteration of empathy
1.4. Visuo-spatial and empathy impairments in schizophrenia: and non-egocentered simulation in schizophrenia remain unknown.
limitations and hypotheses First, Langdon, Coltheart, and Ward (2006) (see also Langdon, 2003,
2006; Langdon & Coltheart, 2001; Langdon et al., 2001) have put for-
Impaired visuo-spatial abilities have been suggested to relate ward that schizophrenics are impaired in spontaneously simulating
with disturbances of empathy under psychotic conditions like another individuals rst-person experience. This hypothesis is com-
schizophrenia (Langdon, Coltheart, Ward, & Catts, 2001; Mohr patible with the patients spontaneous tendency to not disengage
et al., 2010; Thakkar & Park, 2010). Disturbed cognitive functions from themselves as rst reference frame, as reected in increased
generating spatial representations (Franck et al., 2001; Keefe egocentricity biased errors and heightened egocentered simulation
et al., 1995; Park, Puschel, Sauter, Rentsch, & Hell, 1999), spatial (Landgraf et al., 2010). Comparably, low scores on ToM tasks have
attention decits (Amado et al., 2009; Bracha, Livingston, been reported to negatively correlate with high scores to the item
Clothier, Linington, & Karson, 1993; Brugger & Graves, 1997) and lack of spontaneity (N6) of the Positive and Negative Syndrome
bias towards the left side of space (pseudo-hemineglect; Scale (PANSS; Kay, Fischbein, & Opler, 1987) (Abdel-Hamid et al.,
Cavezian et al., 2007) are often observed in schizophrenic patients. 2009), suggesting that the spontaneous features of the socio-behav-
People with high schizophrenia-like traits are impaired in imagin- ioural dysfunction in schizophrenia may be a consistent empirical
ing themselves to be located in the body position of a schematic criterion. Furthermore, this hypothesis partially revises the assump-
human gure (own-body transformation tasks; Mohr, Blanke, & tion by Frith (2004) that automatic empathy processing in everyday
Brugger, 2006), as well as ToM and visuo-spatial tasks, notably interactions (on-line) is preserved, contrasting with break-downs
when they are asked to imagine how locations would appear from in explicit experimental tasks (off-line) due to the fact that
another perspective than their own one (Langdon & Coltheart, patients are not taking part in the interaction and to altered working
1999). Conversely, improved accuracy rates in visuo-spatial memory and meta-cognitive processing on which more weight is
90 B. Thirioux et al. / Brain and Cognition 90 (2014) 8799

put to perform the required explicit task. However, no study to our heterocentered visuo-spatial mechanisms and employ, instead,
knowledge has so far explored the spontaneous visuo-spatial strat- egocentered strategies as in sympathy.
egies associated with empathy in schizophrenia.
Second, experimental-behavioural paradigms assessing empa- 2. Methods
thy are somewhat rare (Bora et al., 2008; Langdon et al., 2006;
Lee et al., 2004; Montag et al., 2007). Measurements of empathy 2.1. Participants
and its associated perspective-change processes are typically based
upon self-rating questionnaires. This is a non-negligible limitation Ten patients with DSM-IV-TR schizophrenia (axis-I disorders;
as patients with schizophrenia generally present poor insight French version of the Diagnostic Interview for Genetic Studies
(Erickson, Jaafari, & Lysaker, 2011; Lysaker, Clements, Plascak- [Numberger et al., 1994]) and ten control volunteers with neither
Hallberg, Knipscheer, & Wright, 2002; Lysaker, Hasson-Ohayon, psychiatric nor neurological history took part in this experiment
Kravetz, Kent, & Roe, 2013). (Table 1). Patients and controls matched for sex (all were males),
Third, robust behavioural data dissociating decits in empathy age (patients: aged 2242 years, 33.3 6.4 years; controls: aged
from decits in sympathy with respect to altered heterocentered 2242 years, 32.5 5.8 years; p = 0.771) and handedness (all were
vs. egocentered visuo-spatial abilities in schizophrenia are still right-handed [Oldeld, 1971]) (Table 1). All had normal or
missing. corrected-to-normal vision.
Considering the three above-mentioned limitations, it remains Patients were recruited among the outpatients and inpatients
unknown whether schizophrenics, when tested in ecologically treated at the Department of Psychiatry of the Henri Laborit Hospital
more valid conditions and taking actively part in self-other interac- (Poitiers, France). Diagnosis of DSM-IV-TR schizophrenia was
tions (on-line conditions), spontaneously use egocentered or het- conrmed by an experienced psychiatrist (L.T.) and two further
erocentered visuo-spatial mechanisms as respectively associated senior psychiatrists. Patients included in the study had a diseases
with sympathy and empathy. Here, we employed our behavioural duration between 6 and 19 years (mean SD years of duration,
paradigm newly validated with non-clinical populations 11.8 1.5 years). Psychopathology was rated by means of the French
(Thirioux et al., 2009, 2010) that enables to test whether individ- version (Guel, 1997) of the Positive and Negative Syndrome Scale
uals are spontaneously interacting with another individual by for schizophrenia (PANSS; Kay et al., 1987). To provide additional
using egocentered (sympathy) or heterocentered (empathy) information on the positive symptoms, the PANSS was completed
visuo-spatial mechanisms. For that, schizophrenic patients, stand- by the clinical dichotomic (yes/no) evaluation of the presence/
ing and moving, interacted with a life-sized virtual tightrope- absence of Schneiders rst-rank symptoms (Farrer & Franck,
walker, standing and moving as well. We predicted that patients 2009). Especially, symptoms 2, 3, and 1519 of the Andreasens posi-
have decits in spontaneous empathy processing and associated tive symptoms evaluation scale (SAPS, [Andreasen, 1981]; French

Table 1
Patients socio-demographic, medical, clinical and psychometric data.

Age Education Chlor. Equ. Diseases Schneid. MADRS PANSS PANSS PANSS Front SPO (OBT- IRI-
(years) (mg) duration Sympt. total positive negative manner)% PT
All patients
P1 28 12 133 6 pres. 13 98 18 39 85.6 15
P2 27 11 1300 7 pres. 10 116 35 26 95.5 20
P3 22 12 200 9 pres. 11 120 15 38 2.2 10
P4 37 12 30 8 abs. 13 93 18 35 0 14
P5 32 11 1533 15 pres. 13 97 36 23 100 9
P6 42 11 520 19 abs. 13 108 20 35 4.5 11
P7 35 15 900 19 abs. 8 70 18 19 97.4 18
P8 41 13 1700 15 abs. 10 96 17 36 0 8
P9 32 10 260 11 pres. 22 118 18 41 0 12
P10 37 11 68 9 abs. 8 88 21 30 94.4 18
mean 33.3 11.8 664.4 11.8 12.1 100.4 21.6 32.2 25 13.5
se 6.4 0.4 203.5 1.5 1.3 4.9 2.4 2.3 15.8 1.3
SCZ-H
P1 28 12 133 6 pres. 13 98 18 39 85.6 15
P2 27 11 1300 7 pres. 10 116 35 26 95.5 20
P5 32 11 1533 15 pres. 13 97 36 23 100 9
P7 35 15 900 19 abs. 8 70 18 19 97.4 18
P10 37 11 68 9 abs. 8 88 21 30 94.4 18
mean 31.8 12 768.8 11.2 10.4 93.8 25.6 27.4 94.7 16
se 2.0 0.8 298 2.5 1.1 7.5 4.0 3.4 2.5 2.0
SCZ-E
P3 22 12 200 9 pres. 11 120 15 38 2.2 10
P4 37 12 30 8 abs. 13 93 18 35 0 14
P6 42 11 520 19 abs. 13 108 20 35 4.5 11
P8 41 13 1700 15 abs. 10 96 17 36 0 8
P9 32 10 260 11 pres. 22 118 18 41 0 12
mean 34.8 11.6 542 12.4 13.8 107 17.6 37 1.34 11
se 3.7 0.5 300 2.0 2.1 5.5 0.8 1.1 0.3 1.0

Socio-demographic (age, education), medical (duration of the disease, daily dosage of chlorpromazine equivalent [Chlr. Equ.]), clinical (presence/absence of Schneiders rst-
rank symptoms [Schneid. Sympt.]), and psychometric (MADRS, total PANSS, positive and negative dimensions on PANSS) data are shown for each patient. Data are rst
presented for all ten patients irrespective of their distribution into groups and, then, for each group (SCZ-H and SCZ-E) separately (mean values and standard errors are
indicated in bold). We further show the percentages of tilts in OBT-manner for the front SPO-task and scores on the IRI Perspective-Taking subscale (IRI-PT) as these differed
between the two groups of patients (for more details, see also Tables 2 and 3).
B. Thirioux et al. / Brain and Cognition 90 (2014) 8799 91

version [Guel, 1997]) were evaluated. At the time of the clinical Software) (images per movie, 37; refresh rate, 100 Hz; movie dura-
examination, ve patients were assessed with positive symptoms tion, 1480 ms). The tightrope walker was designed by using AnyFlo
(P1, P2, P3, P5, and P9). Depressive symptoms were evaluated by System (Bret, 1988) which generates virtual avatars with a neural
the Depression Rating Scale (MADRS; Montgomery & Asberg, network model taking into account the rules of natural movements
1979). All tested patients were treated with stable doses of atypical and biomechanical constraints of the body (2/3 power law;
antipsychotics (chlorpromazine equivalent; CPZ; Woods, 2003) and Berthoz, 1997; Viviani & Flash, 1995; Viviani & Terzuolo, 1982).
stabilized since at least three months (Table 1). Patients with con- To reinforce the ecological aspects of the experiment, the animated
current axis-1 disorders according to DSM-IV-TR criteria, a diseases tightrope walker was further displayed life-sized onto a large
duration superior to 20 years, a stable regime of benzodiazepines screen (2 m  2 m) [naturalistic features]. The tightrope walker
and/or mood stabilizers at the time of the behavioural testing, an was shown standing on a rope with the arms horizontally out-
acute depressive symptomatology, anxiety disorders, sensorimotor, stretched either in front- or back-facing orientation. In each orien-
language production and/or comprehension or other neurological tation, she performed lateral body tilts either to her left or right.
disorders as well as substance-abuse or dependence were systemat- Thus, four movies were presented (front-left; front-right; back-
ically excluded from participation. We here note that, except one left; back-right). In each movie, the onset of the tightrope walkers
patient [P9], all patients obtained low scores on MADRS. We tilt was delayed with respect to the stimulus onset by 50 ms. A trial
included P9 in the study as the clinical examination showed a stable contained one movie and was initiated after a variable interstimu-
mood symptomatology. lus interval (randomly chosen between 500 ms and 2000 ms;
Patients and controls were naive to the purpose of the experi- mean, 1500 ms).
ment and gave written informed consent. The study protocol has Patients and controls stood in front of the screen at a viewing
been approved by the local ethics research committee of the Henri distance of 2 m. To mimic everyday social encounters and
Laborit Hospital and performed in accordance with the ethical strengthen interaction, giving participants the impression to act
standards laid down in the Declaration of Helsinki. in the same spatial environment as the tightrope walker, partici-
pants further stood on a red line (3 m  10 cm; length  width)
2.2. Experimental setup and procedures which prolonged on the ground the avatars rope on the screen.
Moreover, before the movies started, we instructed participants
The paradigm (2.2.1), stimuli (2.2.2) and tasks (2.2.3) that we to stand in the so-called Romberg position (Romberg, 1846) with
employed enable to test participants in ecologically more valid one foot in front of the other on the red line, i.e., in a standing posi-
conditions, approximating daily-life and on-line conditions. For tion approximating the unbalanced position as the tightrope
that, we controlled three key phenomenological aspects of interin- walker, because most social interactions occur in the same body
dividual relationships: interactive, naturalistic and spontaneous position (Bavelas, Black, Chovil, Lemery, & Mullett, 1988; Bavelas,
(for more details, see Thirioux et al., 2009). Black, Lemery, & Mullet, 1987; Parsons, 1987; Reed &
McGoldrick, 2007) [interactive features]. Participants were further
2.2.1. Paradigm asked to choose the most comfortable position (i.e., either with the
Focusing on the visuo-spatial features of empathy and sympa- right or left foot in front of the other). Ten patients and seven
thy, our behavioural paradigm measures from the bodily postures controls chose standing with their right foot in front of the left.
and movements whether individuals, without explicit instruction, Participants held a metal bar (length, 65 cm) horizontally in front
are interacting with another individual by using an egocentered of them and placed their thumbs on two buttons that were posi-
as in sympathy or heterocentered as in empathy reference tioned at the left and right ends of the bar. These buttons were
frame (Fig. 1A). used to record the tilt direction (left or right) and reaction times
If two individuals A (Self) and B (Other) are facing each other (RTs) (Fig. 2).
and B is leaning to his/her right, A can copy Bs tilts by leaning
either to his/her left or right. In the rst case, A reacts by mirroring 2.2.3. Tasks
Bs tilts. This reection symmetry indicates that A, imagining his/ 2.2.3.1. Spontaneous task. To test whether patients with schizo-
her own-body at its actual physical position (embodied self-loca- phrenia spontaneously use egocentered (as in sympathy) or het-
tion) and keeping his/her own visuo-spatial perspective (egocen- erocentered (as in empathy) visuo-spatial mechanisms to interact
tered), is further imagining that Bs tilts are his/her own-body with the avatar, we only instructed them to observe the tilts of
movements as reected in the mirror. This mapping of Bs bodily the tightrope walker and to lean when she was leaning. The exact
movements into As own-body and egocentered transformation instruction was you will see a tightrope walker leaning on a rope.
tend to merge identities between A and B, leading to movements Please lean when she is leaning. No instruction with respect to
self-attribution. Accordingly, reection symmetry reects that A direction of leaning, self-location or visuo-spatial perspective was
is sympathizing with B (or feeling with B, i.e., the same kind of given. This spontaneous task (SPO-task) that allows participants
action-related inner state and at the same time) (Fig. 1A right to use their own transformation and visuo-spatial strategies, com-
column). parable to strategies as used in daily life (spontaneous features),
In contrast, the second case or rotation symmetry indicates was always delivered rst.
that A is imagining himself/herself at Bs body position (disembod-
ied self-location) and adopting Bs visuo-spatial perspective (het- 2.2.3.2. Explicit tasks. To investigate whether the spontaneous
erocentered) by performing a mental transformation of his/her visuo-spatial transformations in self-other interaction are relying
own-body. Accordingly, rotation symmetry reects that A is empa- on the same behavioural mechanisms as explicit egocentered (as
thizing with B (or feeling into B, i.e., with the awareness of being in sympathy) or heterocentered (as in empathy) visuo-spatial
outside B and having to reach her/him while maintaining self-other transformations, patients in the second and third experimental
distinction) (for more details, see Thirioux et al., 2009, 2010, 2014) conditions were explicitly instructed to perform two distinct self-
(Fig. 1A left column). location and visuo-spatial tasks while leaning.
The Mirroring task [MIR-task] (Arzy et al., 2006) tested for
2.2.2. Stimulus and apparatus embodied self-location and egocentered visuo-spatial strategies
Short colour movies of a computer-generated female tightrope in sympathy. The exact instruction was you will see a tightrope
walker were presented using E-Prime Software (Psychology walker leaning on a rope. Please, lean when she is leaning while
92 B. Thirioux et al. / Brain and Cognition 90 (2014) 8799

Fig. 2. Experimental settings and stimuli. (A) Patients and healthy volunteers were facing a large screen and standing in the Romberg position on a line on the ground. They
were holding a metal bar with response-buttons positioned at the left and right ends of the bar, horizontally in front of them. (B) Movie samples as used in the three tasks. A
virtual female tightrope walker, performing whole-body tilts either to the left (L) or right (R) from different orientations (front or back-facing), was shown on the computer
screen and displayed life-sized.

imagining that your body is at its actual physical position and 2.3. Data acquisition and analysis
while keeping your own visuo-spatial perspective. Please, further
imagine that the tightrope walkers tilts are your own-body move- 2.3.1. Behavioural data
ments as reected in a mirror. In both front and back orientations, For each trial, E-Prime recorded the tilt direction (left or right as
we expected a contralateral leaning pattern (i.e., left/right tilt of indicated by button presses) and the reaction time. For each com-
the tightrope walker ? right/left tilt of participants). bination of task (SPO, OBT, MIR) and orientation (front, back), we
The Own-Body Transformation task [OBT-task] (Blanke et al., computed the percentage of tilts according to reection symmetry
2005) tested for disembodied self-location and heterocentered (tilts in MIR-manner) and rotation symmetry (tilts in OBT-man-
visuo-spatial strategies in empathy. The exact instruction was ner). For the MIR- and OBT-tasks, we computed mean RTs for
you will see a tightrope walker leaning on a rope. Please, lean responses in reection and rotation symmetry, respectively. For
when she is leaning while imagining that your body is in the posi- the SPO-task, we calculated the mean RTs for tilts in OBT- or
tion of the tightrope walkers body and while adopting her visuo- MIR-manner (same as in Thirioux et al., 2010).
spatial perspective. An ipsilateral leaning pattern was expected To test for statistical differences between controls and patients,
in both front and back orientations (i.e., left/right tilt of the tight- we rst computed an unpaired 3  2  2 repeated-measures
rope walker ? left/right tilt of participants). ANOVA on the percentage of tilts in OBT-manner with the factor
The order of the MIR- and OBT-tasks was counterbalanced. In all task (SPO, OBT, MIR), orientation (front, back), and group (controls,
tasks, participants were instructed to initiate their tilt with the schizophrenics). The direction of tilts allowed us analysing
same speed as the avatars tilt and to press with their thumb the whether tilts in the SPO-task were similar to those of OBT- or
left or right button of the bar corresponding to the direction of MIR-task (same as in Thirioux et al., 2010). For response speed,
their tilt when they judged that their tilt had arrived at its maximal we calculated an unpaired 3  2  2 ANOVA on the RTs with task,
amplitude. In a training session, before the experiment, partici- orientation and group as factors.
pants were instructed to lean to the left and right and to press Concerning leaning performance, we found a signicant
the corresponding button at the same time. Before task perfor- task  orientation  group interaction attributable to different
mance and after the SPO-task, the MIR- and OBT-tasks were behavioural patterns of half patients in the front SPO-task, differ-
trained in 90 trials. In each MIR- and OBT-task, participants were ing from the remaining ve patients and controls (see
instructed to perform the requested visuo-spatial transformation Section 3.1). Accordingly, we split the patients group into two
while leaning and before giving the response. Each condition con- sub-groups. We calculated 3  2 repeated-measures ANOVAs
tained three blocks. Within a block, in a random order, each of the (with task and orientation as factors) for each group on tilts per-
four movies appeared 15 times, giving rise to 60 trials per block formance and RTs, separately. To test for statistical comparisons
and 180 trials per condition. between groups, we further computed two-tailed unpaired
t-tests.

2.2.4. Interpersonal Reactive Index 2.3.2. Socio-demographic, medical, clinical, psychometric and IRI data
After the recording, all participants completed the French ver- To compare the IRI scores between controls and patients as well
sion of the Interpersonal Reactive Index (IRI; Davis, 1983), a four as socio-demographic (age, education), medical (daily dosage of
7-items subscales self-report assessing empathic abilities. The chlorpromazine equivalent), clinical (duration of the disease, pres-
Perspective-Taking (PT) and Fantasy scales (FS) respectively ence/absence of Schneiders rst-rank symptoms), and psychomet-
measuring the ability to adopt the viewpoint of others in daily-life ric (MADRS, total PANSS, negative and positive dimension on
situations and the tendency to put oneself into the experience of PANSS, IRI) data between patients in both groups, we calculated
ctional characters evaluate the cognitive components of empa- two-tailed unpaired t-tests.
thy (Cognitive Empathy [IRI-CE]). The Empathic Concern (EC) Patients in the second group were found to exhibit higher
and Personal Distress (PD) scales respectively assessing the scores to the negative PANSS than patients in the rst group (see
capacity for concerned and compassionate feelings for others and Section 3.2.2). Thus, to test whether the alteration of spontaneous
the occurrence of self-oriented responses to the negative experi- empathy processing relates or not with the severity of the negative
ences of others evaluate the emotional component of empathy symptomatology, we nally performed a Spearman Rank-Order
(Emotional Empathy; [IRI-EE]). Correlation analysis in all tested patients (N = 10) on the negative
B. Thirioux et al. / Brain and Cognition 90 (2014) 8799 93

PANSS scores and percentages of tilts in OBT-manner in the front followed closely the tilt performance in the OBT-task but differed
SPO-task (see Section 3.2.3). from that in the MIR-task, i.e., all ten participants leaned in OBT-
manner in almost all trials (94.9 2.7%) (Table 2; Fig. 3). This
was conrmed by statistical analyses, showing a signicant effect
3. Results
of task (F(2,18) = 1878; p < 0.001), attributable to a signicant differ-
ence between the OBT- and MIR-tasks (p < 0.001) and SPO- and
3.1. Behavioural results
MIR-tasks (p < 0.001) (post hoc tests; pairwise comparison; least
signicant difference [LSD]). In contrast, the SPO- and OBT-tasks
We rst statistically tested for differences in leaning patterns
did not signicantly differ (p = 0.059). This leaning pattern indi-
between controls and patients. Statistical analyses on tilts percent-
cated that controls have spontaneously used a heterocentered
ages showed a signicant effect of task (F(2,36) = 367.8; p < 0.001)
visuo-spatial referencing to interact with the avatar. Concerning
and orientation (F(1.18) = 7.123; p = 0.006) as well as signicant
RTs, statistical analyses indicated a signicant effect of orientation
task  group (F(2,36) = 7.331; p = 0.002), orientation  group
(F(1,9) = 6.345; p = 0.033), a signicant task  orientation interac-
(F(1,18) = 6.049; p = 0.024), task  orientation (F(2,36) = 9.159;
tion (F(1,9) = 7.123; p = 0.005) and a trend for the factor task
p = 0.001) and task  orientation  group (F(2,36)=9.296; p = 0.001)
(F(2,18) = 3.155; p = 0.067). RTs were faster for the back than front
interactions. The distribution of tilts percentages indicated that
orientation in the OBT- (p = 0.020) and SPO-tasks (p = 0.001). The
the task  orientation  group interaction was due to heteroge-
inverse pattern was found for the MIR-task, although this effect
neous behavioural patterns (rotation vs. reection symmetry) in
failed to be signicant (Table 2; Fig. 3).
the front SPO-task between patients. Accordingly, we split the
patients group into two sub-groups. The rst group included P3,
P4, P6, P8 and P9, and the second group included P1, P2, P5, P7 3.1.2. Schizophrenic patients
and P10 (see Section 3.1.2). The rst group of patients behaved as controls and performed
Concerning RTs, there were a signicant effect of orientation tilts in OBT-manner in the SPO-task (94.9 1.8%), indicating that
(F(1,18) = 12.29; p = 0.003) and signicant task  group they spontaneously used a heterocentered coding (SCZ-H; N = 5).
(F(2,36) = 9.208; p = 0.001) and task  orientation (F(2,36) = 19.06; Patients further leaned correctly in reection and rotation symme-
p < 0.001) interactions. try in the MIR-task (95.2 2.4%) and OBT-task (94.7 4.7%), respec-
tively (Table 2; Fig. 4). Statistical analyses showed a signicant
3.1.1. Control group effect of task (F(2,8) = 320.4; p < 0.001) that was due to a signicant
Controls performed correctly for MIR- and OBT-tasks, leaning difference between the OBT- and MIR-tasks (p < 0.001) and
respectively in reection (97.8 1.0%; mean SD) and rotation SPO- and MIR-tasks (p < 0.001). The SPO- and OBT-tasks did not dif-
(98.3 0.8%) symmetry. The tilt performance in the SPO-task fer (p = 0.942). Statistical analyses on RTs showed a signicant

Table 2
Tilts performance and reaction times.

MIR-task OBT-task SPO-task


Back Front Back Front Back Front
% MIR RTs (ms) % MIR RTs (ms) % OBT RTs (ms) % OBT RTs (ms) % OBT RTs (ms) % OBT RTs (ms)
Controls
C1 100 685 100 666 100 634 90 729 97.8 738 88.9 793
C2 100 749 97.7 596 96.7 698 96.7 847 100 664 97.8 761
C3 100 816 98.8 835 100 825 100 859 100 1145 98.8 1139
C4 98.9 927 98.9 885 100 831 100 856 100 892 94.4 915
C5 94.4 639 87.8 683 98.9 538 94.4 711 64.4 559 98.8 598
C6 96.7 658 96.7 655 98.9 614 100 699 98.9 613 94.4 664
C7 97.8 680 98.9 664 97.8 712 95.6 735 96.7 963 82.2 986
C8 92.2 687 98.9 672 98.9 597 98.9 633 100 622 97.8 705
C9 100 777 100 662 100 780 98.9 767 98.9 796 93.3 834
C10 98.9 900 98.9 915 100 922 100 899 96.7 934 100 969
mean 97.9 752 97.7 723 99.1 715 97.4 773 95.3 793 94.6 836
se 0.9 32 1.1 35 0.4 39 1.0 27 3.5 59 1.7 53
SCZ-H
P1 81.1 1102 91.1 1125 97.7 1042 92.2 1155 93.3 1120 85.6 1270
P2 96.7 1266 91.1 1206 65.5 1198 97.7 1332 91.1 980 95.5 1189
P5 100 1015 98.8 899 98.9 834 100 930 100 708 100 854
P7 98.8 664 96.7 674 97.8 579 100 616 98.8 694 97.4 755
P10 97.8 1135 100 1095 98.8 736 98.8 892 93.3 725 94.4 856
mean 94.9 1036 95.5 1000 91.7 878 97.7 985 95.3 845 94.6 985
se 3.5 101 1.9 96 6.6 110 1.4 122 1.7 87 2.4 102
SCZ-E
P3 60 1279 84.4 1260 97.8 1180 94.4 1169 96.7 970 97.8 955
P4 93.3 877 99 836 100 826 100 869 99 719 100 696
P6 87.3 778 88.9 765 96.6 630 95.5 717 100 519 95.5 497
P8 96.6 998 98.9 945 98.8 1140 85.5 1265 100 784 100 794
P9 98.8 902 100 830 98.8 747 98.8 779 100 743 100 715
mean 87.2 967 94.2 927 98.4 905 94.8 960 99.1 747 98.7 731
se 7.1 86 3.2 88 0.6 109 2.6 109 0.6 72 0.9 74

Percentages of tilts (in MIR-manner for the MIR-task, in OBT-manner for the OBT-task and in OBT- or MIR-manner in the SPO-task) and corresponding reaction times are
shown for each control (C) and patient (P) in each group (SCZ-H and SCZ-E) and for each spatial orientation (back and front). Mean values are also indicated for each task and
orientation (in bold).
94 B. Thirioux et al. / Brain and Cognition 90 (2014) 8799

Fig. 3. Leaning performance and reaction times Control Group. (A) Tilt performance. Results show that healthy volunteers in the SPO-task behaved as in the OBT-task: they
performed tilts in OBT-manner, independently from the stimulus orientation. (B) Reaction times. In general, RTs tended to be longer in the spontaneous (SPO) than explicit
(OBT/MIR) tasks. Moreover, response latencies increased from back to front orientation in the SPO- and OBT-tasks, i.e., when the rotation angle between the participants body
and the avatars body increased. There was no statistical difference between the back and front orientation in the MIR-task.

Fig. 4. Patients leaning performance and reaction times. Tilt performance (left column). (A) Five patients (SCZ-H) behaved as controls: they performed correctly for the OBT-
and MIR-tasks and leaned in OBT-manner for the SPO-task in both front and back orientations. (B) The remaining ve patients (SCZ-E) performed tilts in MIR-manner in the
front SPO-task, differing from controls and the rst group of patients. In contrast, they behaved correctly for the OBT- and MIR-tasks in both orientations and leaned in OBT-
manner for the back SPO-task as controls and SCZ-H. Reaction times (right column). (C) Patients with preserved spontaneous heterocentered processing performed slower in
the front than back orientation for the SPO/OBT-tasks. RTs did not distinguish between the front and back orientations in the MIR-task. (D) Patients with decits in
spontaneous heterocentered processing performed faster in the front than back MIR-task. There was no statistical difference between the front and back orientations in the
SPO- and OBT-tasks.

effect of orientation (F(1,4)=29.47; p = 0.006) and a signicant (p = 0.006) and SPO-task (p = 0.004). RTs were slower in the back
task  orientation interaction (F(2,8)=15.96; p = 0.002). Patients than front MIR-task, although this effect was not signicant
performed faster in the back than front orientation for the OBT-task (Table 2; Fig. 4).
B. Thirioux et al. / Brain and Cognition 90 (2014) 8799 95

Patients in the second group performed tilts in MIR-manner for Table 3


the front SPO-task (98.7 0.9%) indicating that they spontaneously Scores on the Interpersonal Reactive Index.

used an egocentered coding (SCZ-E; N = 5) and distinguishing from IRI-FS IRI-PT IRI-CE total IRI-EC IRI-PD IRI-EE total IRI-TOTAL
controls and the rst group of patients (Table 2; Fig. 4). In contrast, (FS + PT) (EC + PD) (CE + EE)
patients in SCZ-E leaned in OBT-manner for the back SPO-task and Controls
performed correctly for the MIR-task (tilts in reection symmetry: C1 10 22 32 21 3 24 56
90.8 5.4%) and OBT-task (tilts in rotation symmetry: 96.6 1.9%), C2 13 18 31 15 4 19 50
C3 11 10 21 13 14 27 48
as controls and patients in SCZ-H. Statistical analyses showed a sig- C4 15 24 39 20 10 30 69
nicant effect of task (F(2,8) = 194.6; p < 0.001) due to a signicant C5 23 15 38 22 20 42 80
difference between the OBT- and MIR-tasks (p < 0.001) and OBT- C6 12 13 25 16 4 20 45
and SPO-tasks (p < 0.001). There was a signicant effect of orienta- C7 20 21 41 17 19 36 77
C8 8 20 28 25 6 31 59
tion (F(1,4) = 483.1; p < 0.001) and a signicant task  orientation
C9 5 8 13 17 10 27 40
interaction (F(1,4)=307.9; p < 0.001) attributable to a signicant dif- C10 4 20 24 14 2 16 40
ference between the back and front SPO-task (p < 0.001), compared mean 12.1 17.1 29.2 18 9.2 27.2 56.4
to the back and front MIR-task (p = 0.115) and OBT-task (p = 0.096). se 1.9 1.7 2.8 1.2 2.1 2.5 4.6
Concerning RTs, statistical analyses showed a signicant effect of All patients
task (F(2,8) = 8.889; p < 0.009) due to faster RTs in the SPO-task than P1 16 15 31 19 20 39 70
MIR-task (p = 0.003) and OBT-task (p = 0.036). There was a signi- P2 27 20 47 23 18 41 88
P3 10 10 20 20 21 41 61
cant task  orientation interaction (F(1,4) = 11.15; p < 0.001). Post
P4 17 14 31 19 20 39 70
hoc tests showed that RTs were signicantly longer in the back P5 19 9 28 11 16 27 55
than front orientation in the MIR-task (p = 0.002) but did not differ P6 13 11 24 27 12 39 63
between orientations in the OBT-task (p = 0.078) and SPO-task P7 12 18 30 21 13 34 64
P8 4 8 12 8 15 23 35
(p = 0.080), contrasting with the RTs patterns in controls and
P9 5 12 17 15 16 31 48
SCZ-H (Table 2; Fig. 4). P10 19 18 37 19 20 39 76
mean 14.2 13.5 27.7 18.2 17.1 35.3 63
3.1.3. Statistical comparisons between groups se 2.2 1.3 3.2 1.8 1.0 2.0 4.7
Statistical comparisons indicated that the tilt performance did SCZ-H
not signicantly differ for the MIR- and OBT-tasks and the back P1 16 15 31 19 20 39 70
SPO-task between groups (all p > 0.050). In contrast, for the front P2 27 20 47 23 18 41 88
P5 19 9 28 11 16 27 55
SPO-task, there was a signicant difference between controls and
P7 12 18 30 21 13 34 64
SCZ-E (p < 0.001) and between the two groups of patients P10 19 18 37 19 20 39 76
(p < 0.001). Controls and SCZ-H did not signicantly differ mean 18.6 16 34.6 18.6 17.4 36 70.6
(p > 0.050). se 2.5 1.9 3.4 2.0 1.3 2.5 5.6
RTs in the MIR-task were faster in controls than patients leaning SCZ-E
in OBT-manner in the front SPO-task (SCZ-H) (back: p = 0.004; P3 10 10 20 20 21 41 61
P4 17 14 31 19 20 39 70
front: p = 0.005) and patients leaning in MIR-manner in the same
P6 13 11 24 27 12 39 63
task (SCZ-E) (back: p = 0.012; front: p = 0.022). There was no differ- P8 4 8 12 8 15 23 35
ence between patients (back: p = 0.614; front: p = 0.592). Controls P9 5 12 17 15 16 31 48
performed signicantly faster in the front OBT-task than both mean 9.8 11 20.8 17.8 16.8 34.6 55.4
patients groups (SCZ-H [p = 0.0038]); SCZ-E [p = 0.045]). Patients se 2.4 1.0 3.2 3.1 1.7 3.4 6.2

did not differ (p = 0.881). There was no statistical difference Total scores on the Interpersonal Reactive Index (IRI-Total), scores on the cognitive
between groups for the back OBT-task as well as front and back (CE) and emotional (EE) empathy, each CE subscale (Fantasy subscale [FS]; Per-
SPO-task (all p > 0.050). spective-Taking [PT]) and EE subscale (Empathic Concern [EC] and Personal Distress
(PD]) are shown for each control (C) and patient (P) of each group (SCZ-H and SCZ-
E). Mean values for all controls and each patients group are also indicated (in bold).
3.2. Socio-demographic, clinical and psychometric data
controls had signicantly lower IRI-PD scores than SCZ-H
3.2.1. IRI data
(p = 0.005) and SCZ-E (p = 0.014). Patients did not differ (Table 3).
There was no statistical difference on the total-IRI between
groups (all p > 0.050).
Concerning the cognitive component of empathy (IRI-CE), 3.2.2. Patients socio-demographic, medical, clinical and psychometric
scores were signicantly lower in patients leaning in MIR-manner data
in the front SPO-task (SCZ-E) than patients leaning in OBT-manner Socio-demographic (age, and education), medical (daily doses of
in the same task (SCZ-H) (p = 0.019). These scores tended to be chlorpromazine equivalent) and clinical (duration of the disease
higher in controls than SCZ-E (p = 0.089) but did not differ between and presence/absence of Schneiders rst-rank symptoms) vari-
controls and SCZ-H (p = 0.266). Scores on IRI-FS were higher in ables did not statistically differ between groups (all p < 0.050).
SCZ-H than SCZ-E (p = 0.035) and tended to be higher in SCZ-H Concerning psychometric data, patients had similar scores on
than controls (p = 0.067). Controls and SCZ-E did not differ MADRS and total PANSS (all p < 0.050). However, scores on the
(p = 0.477). Concerning the IRI-PT, there was no difference between negative PANSS were higher in patients performing tilts in MIR-
controls and SCZ-H (p = 0.617). In contrast, scores were lower in manner for the front SPO-task (SCZ-E) than patients performing
SCZ-E than SCZ-H (p = 0.049) and controls (p = 0.032) (Table 3). tilts in OBT-manner in the same task (SCZ-H) (p = 0.028). In con-
Regarding the emotional component of empathy (IRI-EE), scores trast, scores on the positive PANSS tended to be higher in the latter
were signicantly higher in patients leaning in OBT-manner in the than the former (p = 0.091) (Table 1).
front SPO-task than controls (p = 0.022) whereas they did not differ
between controls and patients leaning in MIR-manner (p = 0.109). 3.2.3. Spearman Rank-Order correlation analysis
There was no difference between patients groups (p = 0.748). The percentages of tilts in OBT-manner for the front SPO-task
Groups did not differ in the IRI-EC scores (all p > 0.050). In contrast, for all tested patients (N = 10) negatively correlated with the scores
96 B. Thirioux et al. / Brain and Cognition 90 (2014) 8799

on the negative PANSS (rs = 0.837; p = 0.003), i.e., the lower the somewhat faster in the front than back orientation. However, this
percentages of tilts in OBT-manner for the front SPO-task, the effect failed to be signicant. In accordance with previous studies
higher the negative PANSS scores. on self-location (Arzy et al., 2006; Easton et al., 2009; Mohr
et al., 2006; Thirioux et al., 2010), the back MIR-task is the most
complicated of all tested mental own-body transformation tasks
4. Discussion
as it requires to computing a mental translation of ones own-body
by 180 while imagining that the stimuluss back is one own-back
In the present pilot-study, we investigated the egocentered and
as seen in the mirror. This absence of effect conforms to our prior
heterocentered visuo-spatial mechanisms respectively associated
study, reporting that spontaneous heterocentered preference is
with sympathy and empathy in schizophrenia. We predicted that
associated with relative difculties in correctly performing the
patients have decits in spontaneously using heterocentered
back MIR-task (Thirioux et al., 2010). The present data suggest that
visuo-spatial mechanisms and employ preferentially an egocen-
participants may have automatized the task, i.e., leaned correctly
tered referencing to interact with a life-sized avatar. This working
but without performing the requested mental own-body
hypothesis was partially veried. Our main ndings, although still
transformation.
preliminary and needing to be further conrmed on a much larger
sample of patients, suggest that the severity of the negative symp-
4.2. Altered spontaneous heterocentered processing in schizophrenia is
toms in schizophrenia relates with disturbances of spontaneous
partly independent from decits in executive control
heterocentered and empathic processing. These decits were
associated with lower scores to self-reported questionnaire sub-
Similar leaning patterns for the front SPO- and MIR-tasks in the
scales assessing the cognitive components of empathy, namely
second group of patients (SCZ-E) reected that these patients have
perspective-taking. We discuss these data with respect to the
spontaneously kept their egocentered visuo-spatial perspective
relation between impairments in heterocentered referencing,
and sympathized with the avatar. They further performed signi-
empathic abilities and self-regulatory processing in patients with
cantly slower in the back than front MIR-task i.e., as expected
a prevailing negative symptomatology.
for embodied mental transformation (Arzy et al., 2006) differing
from the remaining patients and controls. Moreover, RTs did not
4.1. Distinct spontaneous visuo-spatial referencing in patients with increase from back to front orientation in the OBT-task. Hence,
schizophrenia during self-other interaction the patients inability to spontaneously give up an egocentered ref-
erencing in the front SPO-task was associated with difculties to
Analyses of leaning performance showed that patients distin- correctly perform explicit heterocentered visuo-spatial tasks but
guished into two sub-groups because of inverse behavioural enhanced facilities to explicitly keep an egocentered framework,
responses in the front spontaneous (SPO) task. Half patients as reected in the OBT- (back = front) and MIR-task (back > front)
(N = 5; SCZ-H) behaved as controls. That is, spontaneous visuo- RTs patterns. Taken together, our data are in line with previous
spatial transformations in response to the avatars body tilts work showing that schizophrenics suffer from disrupted visuo-
triggered indistinguishable behavioural patterns as explicit spatial information processing (Keefe et al., 1995; Landgraf,
heterocentered (OBT-task) visuo-spatial transformation. On the Amado, Bourdel, Leonardi, & Krebs, 2008; Park & Holzman, 1992)
contrary, the remaining ve patients (SCZ-E) had decits in and allocentric simulation (Langdon & Coltheart, 2001). Second,
spontaneously using heterocentered visuo-spatial mechanisms. our results reinforce the hypothesis of spontaneous heterocentered
They behaved in the front SPO-task as in the front MIR-task, i.e., perspective-taking and simulation decits in schizophrenia
spontaneously employed egocentered visuo-spatial transforma- (Langdon et al., 2006). We suggest that heterocentered visuo-spa-
tions. Scores on PANSS (Kay et al., 1987) indicated that patients tial and associated empathic abilities may be altered in on-line
with such decits exhibited higher negative symptoms. In contrast, (SPO) conditions (second group) but preserved in explicit (off-line)
the symptomatology was heterogeneous in patients with preserved experimental tasks (OBT) (rst group) in schizophrenics. This par-
spontaneous heterocentered referencing as they suffered from tially modulates, thus, the automatic empathy-related hypothesis
prevailing positive (N = 2), negative (N = 2) or mixed (N = 1) by Frith (2004; see also McCabe, Leudar, & Antaki, 2004).
symptoms. Spearman correlation analysis further showed that Patients were faster in the spontaneous than explicit tasks
the percentages of tilts in OBT-manner in the front SPO-task nega- whereas controls presented the inverse response speed pattern
tively correlated with the negative PANSS scores. (SPO > OBT/MIR). Concordant with our prior work (Thirioux et al.,
This similarity between the SPO- and OBT-tasks replicates our 2010), this suggests that explicit instructions in non-clinical popu-
prior studies with non-clinical populations (Thirioux et al., 2009, lations, probably involving motor preparation, have contributed to
2010). In both tasks, tilts were performed in rotation symmetry reducing the time needed to react. We cannot rule out that these
and RTs were faster for the back than front orientation. This typical increased RTs for the explicit tasks echoed executive control and
increase of response speed supports earlier observations that planning disorders in patients. However, such disturbances cannot
visuo-spatial and body-related mental transformations are fully explain the observed decits. The fact that heterocentered
cognitively more demanding with respect to front-facing stimuli visuo-spatial functions were altered in both spontaneous and
requiring a mental rotation by 180 of ones own-body to align explicit tasks reinforces the hypothesis that impaired heterocen-
it with the target stimuluss body than back-facing stimuli tered simulation may be partly independent from disturbances of
yielding a linear mental projection of the body without egocen- executive and more general cognitive functions.
tered transformation (Arzy et al., 2006; Blanke et al., 2005;
Easton, Blanke, & Mohr, 2009; Mohr et al., 2006; Parsons, 1987; 4.3. Disturbances of spontaneous empathic processing relate with the
Thirioux et al., 2010; Zacks, Rypma, Gabrieli, Tversky, & Glover, severity of the negative symptoms
1999). These behavioural patterns rst suggest that explicit het-
erocentered referencing was presumably not altered in the rst Our results further suggest that impaired spontaneous
group of patients and, second, that these patients, as controls, have heterocentered visuo-spatial functions relate with the severity of
spontaneously empathized with the avatar. the negative symptoms. The patients difculties in inhibiting their
In the front and back MIR-task, patients, again as controls, egocentered perspective and disengaging from themselves are
performed correctly body tilts in reection symmetry and were compatible with the negative PANSS items measuring social
B. Thirioux et al. / Brain and Cognition 90 (2014) 8799 97

withdrawal and restriction in social interaction. Moreover, decits these would differ in that the former and latter are respectively
in spontaneous heterocentered visuo-spatial strategies (SPO-task) associated with heterocentered and egocentered referencing. In
predicted disturbances in explicit heterocentered visuo-spatial their study on schizotypy, Thakkar and Park (2010) provided sim-
tasks (OBT-task). The relation between decits in social cognition, ilar conclusions regarding their paradigm and proposed that exces-
disturbances in visuo-spatial functions and symptomatology sive egocentered referencing as well as decits in non-egocentered
(positive vs. negative) has not been entirely cleared up yet simulation would comparably reduce empathic understanding and
(Abdel-Hamid et al., 2009; Montag et al., 2007; Sergi et al., abilities. New paradigms, inspired from that used in the present
2007). Published data are still misleading, depending on tasks study, should enable to dene empirical criteria distinguishing
and experimental designs. However, prior behavioural studies between normal vs. augmented heterocentered and egocentered
have shown that patients with negative symptoms are more visuo-spatial mechanisms. Moreover, future experiments combin-
impaired in recognizing emotions from facial expressions and in ing visuo-spatial, ToM and emotion tasks, should investigate
more general social abilities, compared to patients with positive whether difculties of patients with negative symptoms in disen-
symptoms (Brne, 2005a; Mueser et al., 1996; Penn, Spaulding, gaging from their egocentered visuo-spatial perspective relate
Reed, & Sullivan, 1996). Preeminent negative symptomatology with the incapacity to take into account the beliefs, desires, and
has been also reported to relate with acuter impairments in ToM emotions of others whereas facilities of patients with positive
performance, specically when the patients symptomatology is symptoms in inhibiting their egocentered reference frame relate
similar to that of autism (Brne, 2005b; Langdon et al., 1997). This with the tendency to overrate and over-attribute intentions,
would be due to that patients with negative features are incapable thoughts etc. to other people.
to represent mental states at all whereas patients with positive
features are altered in ascribing the correct mental state (Frith,
2004). ToM performances under non-pathological conditions rely 4.4. Low scoring self-reported perspective-taking abilities is associated
upon accurate inferences on contextual information, perspective- with altered spontaneous empathic processing
taking and self-other distinction (Walter, 2012). Interestingly,
decits in both visuo-spatial and psychological/cognitive perspec- Patients with decits in spontaneous empathic processing had
tive-taking have been further shown to co-occur in schizophrenia signicantly lower scores on the IRI Perspective-Taking subscale
(Langdon et al., 2006). These ndings are concordant with the than controls and patients with preserved empathic abilities. This
inability of patients with negative features to inhibit their egocen- rst supports the leaning performance and RTs patterns as
tered perspective and to empathize with another individuals observed in the SPO- and OBT-tasks, suggesting that disturbances
rst-person experience in our study. in spontaneous heterocentered and empathic processing are asso-
The symptomatology was not homogenous in the rst group of ciated with low scoring self-reported trait cognitive empathy,
patients (SCZ-H). This is, thus, more difcult to account for the notably perspective-taking. This is further concordant with high
relation between preserved heterocentered processing and dimen- negative PANSS scores found for these patients. Second, although
sions of schizophrenia. Concerning patients with positive symp- schizophrenics have poor insight and decits in the meta-cognitive
toms (N = 2), it could be rst advanced that these were not knowledge of their impairments (Bora et al., 2008), our data
specically impaired in their heterocentered visuo-spatial and indicate that patients may reexively access to their inability to
empathic abilities. However, a recent behavioural work reported simulate a non-egocentered perspective, in accordance with prior
that greater accuracy on perspective -taking and self-location tasks studies (Montag et al., 2007). However, these ndings must be
on front- vs. back-facing human pictures positively correlates with taken with caution as data in the devoted literature are still
increased positive syndrome schizotypy (Thakkar & Park, 2010). equivocal. No clear-cut and stable relationship has been so far
According to the authors, these ndings suggest that schizotypal established between scores to cognitive empathy and perspec-
individuals suffering from anomalous cognitive and perceptual tive-taking subscale, insight and symptomatology (Montag et al.,
experiences have augmented facilities in inhibiting their egocen- 2007). However, negative correlations have been observed
tered perspective (Thakkar & Park, 2010). In the same vein, between perspective-taking and negative symptoms (Brne,
Abu-Akel (1999) hypothesized that patients with preeminent posi- 2005b; Frith, 2004), in line with our data. We here note that the
tive symptoms may have hyper ToM. These augmented if not absence of difference on the IRI-CE scores between controls and
aberrant competences would lead patients to overrate and/or patients with altered spontaneous empathic processing was prob-
over-attribute intentions, thoughts etc. to other people, as reected ably due to that patients and controls, although scoring differently
in delusions (Abu-Akel, 1999; Abu-Akel & Bailey, 2000; Brne, on the IRI-PT, did not differ on the IRI-FS.
2005b).
Two patients with preserved empathic abilities presented a
dominant negative symptomatology. At rst sight, this may con- 5. Conclusions
tradict our above hypothesis that altered spontaneous and explicit
heterocentered visuo-spatial mechanisms relate with the severity In the present pilot-study, we investigated whether spontaneous
of the negative symptoms. However, this objection is not totally empathic and heterocentered visuo-spatial mechanisms are altered
admissible. First, as reported above, we found a highly signicant in schizophrenia. For that, we employed our behavioural paradigm,
negative correlation computed on all ten patients between the measuring from the bodily postures and movements, the spontane-
percentages of tilts in OBT-manner in the front SPO-task and the ous use of egocentered as in sympathy or heterocentered as in
negative PANSS scores. Second, these data may rather point to a empathy reference frame during self-other interaction. We report
potential limitation of our paradigm and employed tasks. Rotation that patients with a prevalent negative symptomatology were
symmetry in the SPO-task, without additional debriengs and/or impaired in spontaneously (on-line) as well as explicitly
associated neuroimaging data, does not enable to distinguish (off-line) simulating a non-egocentered visuo-spatial perspective.
whether participants have imagined themselves in the avatars These decits were associated with lower scoring self-reported trait
body position by performing a mental rotation of their own-body cognitive empathy, namely, perspective-taking. Our ndings
or have mentally rotated the avatars body into their own-body. suggest that the severity of the negative symptoms relates with
In both cases, these body-related visuo-spatial transformations disturbance of spontaneous empathic processing in patients with
would have generated similar ipsilateral leaning patterns. Though, schizophrenia.
98 B. Thirioux et al. / Brain and Cognition 90 (2014) 8799

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