'What is more familiar than I? Self, other and familiarity in schizophrenia

Schizophrenia Research 161 (2015) 501–505

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'What is more familiar than I? Self, other and familiarity in schizophrenia Aurely Ameller a,b,c,⁎,1, Antoine Dereux c,e, Caroline Dubertret c,e,f, Guillaume Vaiva a,b,d, Pierre Thomas a,b,d, Delphine Pins a,b,g a

Université Lille Nord de France, F-59000 Lille, France Laboratoire de Neurosciences Fonctionnelles et Pathologies (LNFP), Université Droit et Santé Lille (UDSL), F-59000 Lille, France AP-HP, Department of Psychiatry, Louis Mourier Hospital, Colombes, France. d Centre Hospitalier Universitaire de Lille (CHULille), Hôpital Fontan, Lille, F-59037 France e INSERM U675-U894, Center of Psychiatry and Neurosciences, Paris, France. f University Paris 7 Denis Diderot, Faculty of Medicine, Paris, France. g Centre National de la Recherche Scientifique (CNRS), F-75794 Paris, France b c

a r t i c l e

i n f o

Article history: Received 13 January 2014 Received in revised form 2 December 2014 Accepted 6 December 2014 Available online 19 December 2014 Keywords: Familiarity Capgras Self Schizophrenia Skin conductance response

a b s t r a c t Background: Familiarity disorders (FDs) critically impact social cognition in persons with schizophrenia. FDs can affect both relationships with people familiar to the patient and the patient's relationship with himself, in the case of a self-disorder. Skin conductance response (SCR) studies have shown that familiar and unknown faces elicit the same emotional response in persons with schizophrenia with FD. Moreover, in control subjects, one's own face and familiar faces have been shown to activate strongly overlapping neural networks, suggesting common processing. The aim of the present study was to determine whether the mechanisms involved in processing one's own and familiar faces are similarly impaired in persons with schizophrenia, suggesting a link between them. Method: Twenty-eight persons with schizophrenia were compared with twenty control subjects. Three face conditions were used: specific familiar, self and unknown. The task was to indicate the gender of the faces presented randomly on a screen during SCR recording. Face recognition was evaluated afterwards. Results: Control subjects exhibited similar SCRs for the familiar and self-conditions, which were higher than the responses elicited by the unknown condition, whereas persons with schizophrenia exhibited no significant differences between the three conditions. Conclusion: Persons with schizophrenia have a core defect of both self and familiarity that is emphasised by the lack of an increased SCR upon presentation with either self or familiar stimuli. Familiarity with specific familiar faces and one's own face may be driven by the same mechanism. This perturbation may predispose persons with schizophrenia to delusions and, in particular, to general familiarity disorder. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Since the early 20th century, familiarity disorders (FD) have been described as a failure of affective judgement (Capgras and Reboul-Lachaux, 1923) capable of strongly impacting social interactions. More recently, the literature on schizophrenia has provided evidence for a defect in the feeling of familiarity in front of familiar individuals, despite preserved recognition (Ellis et al., 1997; Hirstein and Ramachandran, 1997). Indeed, by using the skin conductance response (SCR) as a somatic indication of Abbreviations: SCR, skin conductance response; FD, familiarity disorders; μS, microsiemens. ⁎ Corresponding author at: Laboratory of Functional Neurosciences and Pathologies, Service EFV, Hôpital Roger Salengro, CHRU de Lille — CS 700001 — 59037 Lille Cedex, France. Tel.: +33 320 44 59 62/39534; fax: +33 320 44 67 32. E-mail address: [email protected] (A. Ameller). 1 Permanent address: Hôpital Louis Mourier, 178 rue des Renouillers — 92700 Colombes, France. Tel.: +33 1 47 60 64 09; fax: +33 1 47 6067 40.

http://dx.doi.org/10.1016/j.schres.2014.12.007 0920-9964/© 2014 Elsevier B.V. All rights reserved.

emotional arousal, these studies highlighted a lack of emotion elicited by familiar faces in persons with schizophrenia with FD, even though the patients were able to process visual facial features and to recognise their own and familiar faces (Joshua and Rossell, 2009). FD has been described as both a self-centred expression of delusion, in which patients do not express a feeling of familiarity in front of their own face, or as subjective double syndrome, in which they recognise a physical double of themselves in strangers (Luauté and Bidault, 1994; Luauté, 2009). Despite the growing literature suggesting that schizophrenia is essentially a self-disease (for a review see Nelson et al., 2014a, b), only a few studies have focused on the ability to recognise one's own face compared with familiar faces in schizophrenia (or in schizotypy), and the studies performed did not reach a clear consensus. Indeed, although some of these studies suggest a general deficit in self-awareness unrelated to familiarity (Kircher et al., 2007; Lee et al., 2007; Yun et al., 2014), others support a general impairment in familiarity including the familiarity of the self, instead of deficits in self-

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awareness alone (Irani et al., 2006; Caharel et al., 2007; Zhang et al., 2012). In addition, these studies have potential biases. First, an explicit judgement of the self or familiarity was required (Caharel et al., 2007; Kircher et al., 2007; Zhang et al., 2012). This implies conscious processes that could not be involved in familiarity, which is described as a relatively fast and automatic process (Yonelinas and Jacoby, 1994). Second, famous rather than specific familiar (e.g., relatives or friends) faces were used (Lee et al., 2007; Zhang et al., 2012; Yun et al., 2014). This is an important psychopathological point because famous or widely known individuals do not induce FD in persons with schizophrenia (Capgras and Reboul-Lachaux, 1923). Moreover, different forms of declarative memory have been shown to be involved depending on the stimulus type. Specific familiarity, including familiarity with self, involves episodic or autobiographical memories, whereas famous individuals recruit semantic memories (Gillihan and Farah, 2005). Finally, the neural circuitry involved in the processing of one's own face and familiar faces strongly overlaps (mainly in the temporo-parietal junction), highlighting the link between them, whilst the processing of a famous face recruits different cortical regions (Qin and Northoff, 2011). In the present study, we characterised the affective processing involved in both self and familiarity disorders in persons with schizophrenia using SCR recordings in an implicit task on specific familiar (including self) and unknown faces. Under the assumption that in face recognition, the self will be recognised as familiar, it was expected that persons with schizophrenia would exhibit the same lack of emotional arousal in front of themselves as when facing specific familiar individuals.

The average luminosity and contrast were equalised across the faces. A total of 5 static greyscale pictures were presented, 2 in both the familiar and unknown conditions and one in the self-condition. 2.3. Procedure

2. Experimental materials and methods

To assess the affective processes involved in face processing, SCR was recorded during a gender task within the three familiarity conditions. During each trial, a central fixation cross was presented for 2000 ms to alert the participant to the imminent appearance of the stimulus. The face was then displayed until the participant responded. The two specific familiar and the two unknown faces were displayed four times, whereas the participant's own face was displayed eight times. Stimuli were displayed on a computer screen (Intel computer, Sony screen, resolution 1280 × 1024 pixels, refresh rate 60 Hz) in a random order using E-Prime software (Schneider et al., 2012). To avoid SCR habituation effects, the interval between two successive stimuli randomly varied between 8 and 18 s. All of the participants placed their head on a chin rest with their eyes positioned centrally 60 cm from the monitor. All of the faces overlaid a 9.5 × 11° visual angle. During each trial, the participants were asked to indicate the gender of the face displayed as quickly as possible. A response was entered by pressing one of two keys on a keyboard: “1” if the stimulus was a man and “2” if it was a woman. At the end of the experiment, the participants had to indicate, in the absence of SCR recording, the name of each individual they recognised. The whole task was run in a dark room and took approximately 15 min to complete.

2.1. Participants

2.4. Data recording and analysis

Twenty-eight persons (10 women and 18 men) with schizophrenia or schizoaffective disorder as defined by the DSM IV (APA, 2000) were compared with twenty healthy controls (12 women and 8 men) with no psychiatric disorders, as assessed by the Mini International Neuropsychiatric Interview (MINI; Sheehan et al., 1998). Exclusion criteria included: having an axis I or axis II diagnosis (DSM IV), being age the under of 18 or above the age of 55, or having a medical history of sensory or neurological disorders. All subjects provided written consent prior to participation. For the patients with guardianship, the guardians were systematically informed and provided oral consent; no patients with tutors were included. The study was approved by the local ethics committee (CPP Nord-Ouest IV, France). Symptom severity in the patients was assessed with the Positive and Negative Syndrome Scale (PANSS; Kay et al., 1987; Lançon et al., 1997). Self-disorder was assessed in the persons with schizophrenia using the Self-Face Recognition Questionnaire (SFRQ), a scale initially validated for schizotypy (Larøi et al., 2007). Finally, global functioning of the patients was assessed with the Clinical Global Impression (CGI) Scale (Haro et al., 2003).

2.4.1. Behavioural data The response accuracy (man/woman) in the gender task was recorded for each stimulus. Afterwards, correct and false recognitions were rated as “1” or “0”, respectively, for each face.

2.2. Stimuli Stimuli were individually tailored for each participant and consisted of a series of full-frontal high-quality colour photographs of neutralemotion faces (mouth closed). Each face belonged to one of the 3 following conditions: own face, familiar face and unknown face. Two relatives' faces were acquired on a digital camera (iPhone 4S camera, 8 megapixels). A face was considered “familiar” if it had been encountered by the participant at least once each week for a minimum of 6 months. A photograph of each subject was taken as the “self” picture. Unfamiliar faces were chosen from among the Karolinska Directed Emotional Faces (Lundqvist et al., 1998; Goeleven et al., 2008). Using Adobe Photoshop, the faces were cropped along the face contour so that minimal hair or external cues were visible, with the resulting images subtending 250 pixels in width and 335 pixels in height. The faces were displayed in greyscale on a grey background.

2.4.2. SCR data SCRs were recorded during the gender task only. A commercial skin conductance sampling device (BiopacMP35, Biopac Systems Inc., Goleta, Canada) was used with a constant-voltage method (0.5 V) at a sampling rate of 600 Hz. Ag–AgCl electrodes filled with a 0.05 M NaCl electrolyte solution were attached to the palm side of the middle phalanges of the second and third fingers of the participants' hands. Then, SCRs were measured using BSL-pro software©. SCRs were determined using the standard latency criterion of 1–4 s. The first peak of amplitude within this latency window was recorded. Trials for which the stimulation did not produce a peak in SCR were included in the mean data for each participant; in these cases, we considered the SCR value to be zero. The magnitude and the latency of the SCRs were measured. To normalise the data, the amplitude of the SCR measurement was logarithmically transformed [log(1 + amplitude)] and statistical analyses were conducted on the magnitude based on the average SCR amplitude calculated afterwards (Dawson et al., 2000; Boucsein et al., 2012). 2.4.3. Statistical analysis All statistical analyses were performed using SPSS 15.0 and the level of significance was set at p = 0.05. Greenhouse–Geisser corrected repeated measures ANOVA was applied to behavioural responses in the gender and recognition tasks and to SCR data in the gender task only. The patient mental health status (healthy controls, persons with schizophrenia) was selected as the between-subjects factor and the familiarity condition (specific familiar, self, and unknown) was selected as the within-subjects factor. Specific group or condition comparisons were conducted using Student's t-tests. Spearman's correlations were run between the SCR magnitude and age, antipsychotic dosage, benzodiazepine dosage, symptom severity, the CGI and the SFRQ.

A. Ameller et al. / Schizophrenia Research 161 (2015) 501–505

3. Results

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Table 2 Percentages of correct responses (with standard deviations) for both participant groups (control subjects: controls and schizophrenia patients: patients) in the gender task and in the identification task at the end of the experiment.

3.1. Demographic data Table 1 presents the gender and the mean age of the participants as well as the mean scores obtained by the persons with schizophrenia for the different clinical scales and the mean dosages of psychotropic medication. The 2 groups did not differ in gender or age. All patients received second-generation antipsychotic medication (from 33 to 1600 mg chlorpromazine equivalent, median 400 mg); half of the patients (N = 14) were on benzodiazepine medication (from 0 to 50 mg of diazepam equivalent, median 5 mg). 3.2. Behavioural data The proportion of correct responses is presented in Table 2. All participants were able to categorise faces as male or female with more than 85% accuracy for each condition. There was a trend-level group effect on accuracy (F(1,46) = 3.49; p = 0.06), a trend towards a familiarity condition effect (F(2,92) = 2.49; p = 0.058), and a trending interaction between the groups and familiarity conditions (F(2,92) = 2.68; p = 0.06). At the end of the experiment, both participant groups were equally able to identify specific familiar or self faces and unable to identify unknown individuals (t(46) = 1.228; p = 0.227). 3.3. SCR data Global results did not show a familiarity condition effect (F(2,92) = 0.22; p = 0.07), but there was a group effect (F(1,46) = 10.08; p = 0.003) on the SCR magnitude and a significant interaction between the groups and familiarity conditions (F(2,92) = 3.91; p = 0.02). Indeed, the results showed a significant difference between the control subjects and the persons with schizophrenia for specific familiar faces (t(46) = 1.946; p = 0.05) and their own faces (t(46) = 3.336; p = 0.002) but not for unknown faces (t(46) = -0.566; p = 0.623; see Fig. 1 and Table 3). The control subjects showed an overall significant effect of the familiarity conditions (F(2,38) = 3.725; p = 0.03). Higher SCR magnitudes were found in the specific familiar condition than in the unknown condition (t(19) = 2.514; p = 0.02) as well as in the self condition than in the unknown condition (t(19) = −2.153; p = 0.04). However, no difference was found between the specific familiar and the self conditions (t(19) = 0.113; p = 0.912). Persons with schizophrenia exhibited no global effect of the familiarity conditions (F(2,54) = 1.370; p = 0.263). Thus, the SCR magnitudes did not differ between conditions. After splitting the patient group into subgroups of patients on and off benzodiazepine medication (n = 14 in each group), a new analysis was conducted. Within these 2 groups, no familiarity condition effect (F(2,52) = 1.402; p = 0.7255), no group effect (F(1,26) = 1.353; p = 0.255), and no interaction between both (F(2,52) = 1.631; p = 0.206) were revealed.

Gender task

Identification task

Familiar Self Unknown % correct

Controls

Patients

97 ± 6 97 ± 7 97 ± 13 98 ± 0.06

89 ± 11 99 ± 3 86 ± 3 94 ± 0.14

No significant correlations were found between the SCR magnitude in the 3 familiarity conditions and age, neuroleptic dosage, benzodiazepine treatment or the PANSS, SFRQ or CGI scores of the persons with schizophrenia. Moreover, when these variables were introduced as covariates, they did not modify the results described above. Afterwards, to ensure that anticholinergic effects of the medications did not affect SCR data, all the patients' medications were classified in one of the 4° of potential anticholinergic power (ranging from three for “high potential” to zero for “no anticholinergic effect scientifically proven”) in accordance with a review initially conducted for geriatric use of medications with anticholinergic properties (Boily and Mallet, 2008). This variable was then used as a covariate in the ANOVA, with no consequence for the results. 4. Discussion To our knowledge, this is the first study to assess the SCR to one's own face and familiar faces in both healthy control and persons with schizophrenia groups. Our data have demonstrated a reduced SCR in the persons with schizophrenia for the self face and familiar faces compared with the control subjects, whereas no difference appeared between both groups for unknown faces. Thus, although the SCR increased in the healthy subjects for familiar faces and the self face compared with unknown faces, the lack of difference between the 3 conditions in the persons with schizophrenia suggests an emotional numbing, despite accurate recognition and identification. Thus, our results emphasised the dissociation between conscious recognition of faces and the absence of emotion linked to them in schizophrenia. According to the 2-step theory (Coltheart et al., 2011, 2010), this discrepancy between visual feature recognition of faces and an associated experience of emotion may be explained by an impairment in a lowlevel step (as opposed to a complex, integrated, high-level step). Such a disorder would be necessary but insufficient to generate delusions.

Table 1 Mean demographic data (with standard deviations) for the 2 groups. The 2 groups described in the table are control subjects (controls) and persons with schizophrenia (patients). y.o.: years old.

Age Sex PANSS+ PANSS– PANSS G PANSS total SFRQ CGI Diazepam equivalent Chlorpromazine eq.

Controls

Patients

p

34.5 ± 9.5 y.o. 8♂ 12♀

39.5 ± 10.9 y.o. 18♂ 10♀ 13.8 ± 4.6 15.1 ± 5.8 28.8 ± 6.8 57.8 ± 13.4 7.1 ± 7.5 3.3 ± 1.1 10.4 ± 15.5 mg (n = 14) 463.9 ± 346.3 mg

0.10 0.10

Fig. 1. Magnitude of the skin conductance responses in μS with standard deviation bars for the 3 conditions (familiar, self and unknown) for the 2 groups: control subjects in black, persons with schizophrenia in grey. * indicates significant differences in SCR magnitude between groups in both familiar and self conditions (p b 0.05).

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Table 3 Mean SCR magnitude in μS (with standard deviations) for both participant groups (control subjects: controls and schizophrenia patients: patients) in the 3 conditions of the gender task.

Familiar Self Unknown

Controls

Patients

0.08 ± 0.044 0.08 ± 0.047 0.06 ± 0.034

0.05 ± 0.05 0.04 ± 0.042 0.07 ± 0.098

Indeed, such an ambiguity can occur in any individuals, who can then reorient their emotions towards a more plausible conclusion. Persons with schizophrenia would be unable to resolve this ambiguity by adjusting their error, leading them to a delusion. This is this second step in predicting the emergence of delusion. In contrast to previous studies using passive viewing (Ellis et al., 1997; Hirstein and Ramachandran, 1997), the gender task was designed to ensure that the participants' attention was oriented to the faces during their presentation. Indeed, the task was performed with a high level of accuracy in both groups. Nevertheless, a trend towards significance was observed between the control and patient performances. Such a result could be explained by the constraint of using a small number of stimulus repetitions, which was necessary to avoid SCR habituation during the experiment. Conversely, the same argument could also account for the effect of specific familiar faces observed on SCR magnitude at the limit of significance (p = 0.05) between both groups. Additionally, performances exhibited greater variability in the persons with schizophrenia group than in the healthy control group, as observed in previous studies both in motor (Karantinos et al., 2014) and cognitive tasks (Shin et al., 2013). Variability is supposed to reflect the instability of the processes underlying the task (Berberian and Cleeremans, 2010; Kanai and Rees, 2011) and has even been proposed as the best way to distinguish normal from pathological members of the population, such as individuals with attention deficit hyperactivity disorder (Di Martino et al., 2008). In our study, variability in the SCR could reflect the instability of affective processes in schizophrenia. On one hand, the absence of increasing emotional arousal in front of specific familiar faces in schizophrenia agrees with previous SCR studies using familiar (famous) and unknown faces to test patients with FD (Ellis et al., 1997; Hirstein and Ramachandran, 1997). It suggests an FD based on a lack of emotional reactivity to such stimuli in persons with schizophrenia. On the other hand, our study shows a similar lack of emotional arousal in patients presented with their own face, suggesting a defect in self-processing in terms of minimal self (i.e., feeling oneself as experiencing the here and now; Gallagher, 2004). Such a result agrees with the disorder of self-experiences described in schizophrenia (Bleuler, 1911), in terms of either self-recognition (Kircher et al., 2007; Lee et al., 2007; Zhang et al., 2012; Yun et al., 2014) or self-awareness (Bulot et al., 2007; Thakkar et al., 2011) and, above all, in self-related tasks (for a review, see Hur et al., 2014). This decreasing emotional response to a patient's own and familiar faces in patients and healthy subjects' eliciting a high and identical response for both suggests that both types of response are based on the same process, which is disrupted in schizophrenia. The self is familiar, as it is highly known and learned through everyday social interactions that solicit empathy. Our results suggest, then, that we have explored the familiar component of the self. However, the self as a whole is a broader, multimodal, integrated process (Uddin et al., 2005; Tsakiris, 2008; Jardri et al., 2011). The concept of the self (Gillihan and Farah, 2005) includes a physical (e.g., body and face) and a psychological self. The psychological self contains both semantic and episodic memories and the first-person perspective experience. A broader definition of the self includes not only these physical and psychological dimensions but also personal relationships with other individuals. Indeed, repeated interactions with the same people led to not only enhanced representations of these individuals but also the subject's own representation. Neuroimaging studies support this link

between self and familiarity. Indeed, an fMRI meta-analysis of healthy subjects suggested an overlap between the familiarity and self-networks (Qin et al., 2012), especially within the temporo-parietal junction (bilaterally), which is involved (in the right hemisphere) in empathy and in the distinction between self and others. Our study therefore suggests a possible disruption of the distinction between self and others. Even so, further studies will be useful to link the impairment in schizophrenia to the temporo-parietal junction. Benzodiazepines have been linked to a lack of the SCR (Marcy et al., 1985; Siepmann et al., 2007), with more extinction and habituation (Graeff et al., 2003). In our study, the results showed no link between SCR and benzodiazepine treatments. Additionally, anticholinergic drugs are supposed to disturb SCR generation (Dawson et al., 2000; Boucsein et al., 2012). Unfortunately, there is no quantitative measure of the anticholinergic power of drugs. To control for this factor, we used a classification of the potential anticholinergic power of drugs proposed in a previous study (Boily and Mallet, 2008). The results of this analysis suggest that pharmacological treatments are not the causal factor of SCR variation in our study. Eye tracking was not recorded during the task. One might think that the facial scanning patterns could have differed between the patients and the controls and that the patients in our study did not process the relevant facial features. Indeed, it has been shown that persons with schizophrenia have distorted scan paths and elicit reduced attention to salient facial features compared with healthy controls (Phillips and David, 1998; Loughland et al., 2002). Nevertheless, Delerue et al. showed that this was true in only passive viewing tasks (Delerue et al., 2010). Indeed, they showed that scan paths and fixation did not differ between persons with schizophrenia and controls when participants were asked to determine the facial expression, gender, age or familiarity of the face. Thus in our study, the difference in SCR between the persons with schizophrenia and the healthy controls would not be attributable to a difference in face exploration. This study highlights that self and familiarity were both affected in persons with schizophrenia by a decrease in emotional arousal, which may be a core defect in schizophrenia. A functional impairment in the overlap between the self and familiar mechanisms would predispose persons with schizophrenia to delusions of familiarity or of the self (i.e., first-rank symptoms; Lake, 2012). Funding source This work has been conducted without funding sources. Contributors Aurely Ameller and Delphine Pins planned the study. Aurely Ameller designed the study and wrote and programmed the protocol. Aurely Ameller and Antoine Dereux screened the control and patient groups and ensured that the participants completed the task. Aurely Ameller conducted the data analysis. Aurely Ameller and Delphine Pins discussed the results. All authors contributed and have approved the final manuscript. Conflict of interest No authors have conflicts of interest.

Acknowledgement Thanks to Fabien D'hondt for his advices in SCR methods.

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