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Reward modulates the mirror neuron system in schizophrenia: A study into the mu rhythm suppression, empathy, and mental state attribution ab

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Elliot C. Brown , Cristina Gonzalez-Liencres , Cumhur Tas

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& Martin Brüne

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Maryland Psychiatric Research Centre, University of Maryland School of Medicine, Baltimore, MD, USA b

Division of Cognitive Neuropsychiatry and Psychiatric Preventive Medicine, LWL University Hospital, Ruhr University Bochum, Bochum, Germany c

International Graduate School of Neuroscience (IGSN), Ruhr University Bochum, Bochum, Germany d

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Department of Psychology, Üsküdar University, Istanbul, Turkey Published online: 14 Jun 2015.

To cite this article: Elliot C. Brown, Cristina Gonzalez-Liencres, Cumhur Tas & Martin Brüne (2015): Reward modulates the mirror neuron system in schizophrenia: A study into the mu rhythm suppression, empathy, and mental state attribution, Social Neuroscience, DOI: 10.1080/17470919.2015.1053982 To link to this article: http://dx.doi.org/10.1080/17470919.2015.1053982

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SOCIAL NEUROSCIENCE, 2015 http://dx.doi.org/10.1080/17470919.2015.1053982

Reward modulates the mirror neuron system in schizophrenia: A study into the mu rhythm suppression, empathy, and mental state attribution Elliot C. Brown1,2, Cristina Gonzalez-Liencres2,3, Cumhur Tas3,4, and Martin Brüne2,3

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Maryland Psychiatric Research Centre, University of Maryland School of Medicine, Baltimore, MD, USA 2 Division of Cognitive Neuropsychiatry and Psychiatric Preventive Medicine, LWL University Hospital, Ruhr University Bochum, Bochum, Germany 3 International Graduate School of Neuroscience (IGSN), Ruhr University Bochum, Bochum, Germany 4 Department of Psychology, Üsküdar University, Istanbul, Turkey

Impairments in the mirror neuron system (MNS) have been implicated as a possible underlying neurological basis for deficits in higher-level social cognition in schizophrenia. Previous work testing this hypothesis has used the electroencephalographic mu rhythm as an index of MNS activity, with studies showing mixed results. Here we investigated the role that reward plays in modulating the mu rhythm, and its association with empathy and emotional mental state reasoning. A group of schizophrenia patients and a healthy control group completed an action observation paradigm in which they watched actions that were financially rewarding, punishing, or neutral. Patients showed intact reward-related modulation of the mu rhythm, and greater mu suppression was associated with greater negative symptoms. There was also a trend for reduced mu suppression in patients. Furthermore, both empathy and emotional mental state reasoning were associated with the degree of mu suppression, but only in healthy controls. These findings confirm the association between the mu suppression and high-level social cognition. It is possible that schizophrenia patients utilize different cognitive routes to infer mental states. The demonstration that reward influences the degree of mu suppression in schizophrenia patients may help to account for previous conflicting findings in the literature.

Keywords: Schizophrenia; Action observation; EEG; Social cognition; Perspective-taking.

Schizophrenia is characterized by impaired social functioning, which often precedes illness onset, and can predict prognosis (Green & Leitman, 2008). Social cognition includes emotion processing, theory of mind, social perception, and attributional biases, which account for a substantial proportion of the variance in social functioning in schizophrenia

(Brüne, Abdel-Hamid, Lehmkämper, & Sonntag, 2007; Lysaker, Davis, & Hunter, 2004; Penn, Corrigan, Bentall, Racenstein, & Newman, 1997). Antipsychotic pharmacological treatment seems to have little impact on the remission of social impairments (Penn et al., 2009), although there is still little known about the neurological basis of deficits in

Correspondence should be addressed to: Elliot C. Brown, Maryland Psychiatric Research Centre (MPRC), Department of Psychiatry, University of Maryland School of Medicine, 55 Wade Avenue, P.O. Box 21247, Baltimore, MD 21228, USA. E-mail: [email protected] No potential conflict of interest was reported by the authors.

© 2015 Taylor & Francis

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BROWN ET AL.

social cognition in schizophrenia (Brunet-Gouet et al., 2011). One brain network involved in social cognitive processes is the parieto-frontal mirror neuron system (MNS), which is activated during the execution of one’s own actions, as well as through the observation of others’ actions (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996). The MNS is thought to have a central role in the underlying neural basis for higherlevel processes involved in the understanding of others’ goal-directed actions and behaviors (Rizzolatti & Sinigaglia, 2010). Evidence for an electrophysiological index of MNS activity in humans has come from the electroencephalographic (EEG) mu rhythm (8–13 Hz and ~20 Hz) in which a relative suppression or reduction in mu power occurs over sensorimotor cortex during both the execution and observation of actions (Hari, 2006). Correlations between mu suppression and fMRI BOLD signals in MNS regions have corroborated the putative association between the mu suppression and the MNS (Arnstein, Cui, Keysers, Maurits, & Gazzola, 2011; Braadbaart, Williams, & Waiter, 2013). Some authors have made the proposal that a potential deficit in the MNS may contribute to explaining deficits in higherlevel social cognitions (Arbib & Mundhenk, 2005; Enticott et al., 2008), but this relationship has barely been studied. A number of neuroimaging studies have provided support for the suggestion of a dysfunctional MNS in schizophrenia (Lee, Chun, Yoon, Park, & Kim, 2014; Mehta, Thirthalli, Basavaraju, Gangadhar, & Pascual-Leone, 2013; Thakkar, Peterman, & Park, 2014). One mu rhythm study from Singh, Pineda, and Cadenhead (2011) had healthy controls and firstepisode schizophrenia patients observe videos of different actions and found lower mu suppression in the patient group. They also found that patients with less mu suppression exhibited greater anhedonia as well as poorer social adjustment. Another study (McCormick et al., 2012) reported greater mu rhythm suppression in actively psychotic patients, as compared to those with residual symptoms and healthy controls. Psychotic symptoms were also correlated with mu suppression. In contrast, Horan, Pineda, Wynn, Iacoboni, and Green (2014) demonstrated that schizophrenia patients did not exhibit differences in mu suppression across a number of different action observation conditions with differing degrees of social interaction. These conflicting results encourage further exploration, and also beg the question of whether there may be other underlying factors driving these inconsistencies in the mu suppression data.

One possible clue for the inconsistent findings in the literature comes from early work in social learning theory, which argues that the rewarding features associated with others’ actions/behaviors can predict the tendency to imitate the observed action/behaviors (Bandura & Mcdonald, 1963). Further to deficits in social cognition, selective abnormalities in reward processing are also present in schizophrenia and are thought to have some causal role in the expression of psychotic negative symptoms (Dowd & Barch, 2010; Gold, Waltz, Prentice, Morris, & Heerey, 2008; Strauss, Waltz, & Gold, 2014). There is one study showing that impaired empathy (at least self-reported empathic abilities) in schizophrenia is associated with more severe negative symptoms (Konstantakopoulos et al., 2014), which might provide some evidence to relate psychotic symptoms to MNS function. More research has recently been emerging to confirm the rewarding nature of social interactions, as several neuroimaging studies have demonstrated the activation of reward centers during different types of social interaction, with many suggesting an integral role for reward processing in social learning processes (BáezMendoza & Schultz, 2013; Fareri, Niznikiewicz, Lee, & Delgado, 2012; Gariépy et al., 2014). If reward does play a role in social interaction and in promoting social goal-seeking and social motivation, then a deficit in reward processing is also likely to have a detrimental impact on social functioning and the acquisition of social skills. A study from our group (Brown, Wiersema, Pourtois, & Brüne, 2013) demonstrated that the mu suppression is modulated by rewards associated with the observed action, whereby greater mu suppression is evoked when observing actions that are financially rewarding for the observer. Thus it follows that if reward plays a role in the magnitude of mu rhythm suppression, then a deficit in reward processing may also have a detrimental impact on motor resonance during action observation, which has not previously been accounted for. The aim of this study was to investigate the interaction between reward and the mu rhythm suppression during action observation in schizophrenia. A second aim was to investigate the possible effects of perspective on the mu suppression, i.e., the perspective from which the action is seen (first- or third-person perspective), due to the known problems in distinguishing between self and other seen in schizophrenia. It was predicted that there would be an overall reduced mu rhythm suppression in schizophrenia. We also hypothesized that the modulating effects of the reward and perspective conditions on the mu suppression would be different in the patient group, as compared to healthy controls. As a further hypothesis, it was

MU RHYTHM & REWARD IN SCHIZOPHRENIA

predicted that the degree of mu suppression would be associated with self-reported empathy, affective mental state reasoning, and negative symptoms in patients.

METHOD

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Participants Seventeen right-handed participants (nine male) diagnosed with schizophrenia were recruited from the LWL University Hospital Bochum. Diagnosis was confirmed with the ICD (International Classification of Diseases)-10 RDC (Research Diagnostic Criteria). All patients were considered as clinically stable by the consulting psychiatrist and if the dose and type of antipsychotic medication had not changed within the last 6 months. Suitability for participation in the research study was determined by the psychiatrist responsible for the patient. Inclusion criteria for the patient group only permitted the selection of participants who had received a diagnosis of a schizophrenia disorder (ICD-10) that was not drug-induced, had no history of neurological injury, had no obvious motor deficits, and was not currently diagnosed with substance dependence/abuse. Psychotic symptomatology of participants was assessed with the Positive and Negative Syndrome Scale (PANSS; Kay, Fiszbein, & Opler, 1987). The PANSS is a 30-item semi-structured interview designed to assess symptom categories associated with schizophrenia. Five symptom dimension factors were calculated from PANSS scores (Mass, Schoemig, Hitschfeld, Wall, & Haasen, 2000), with factors being hostile excitement, negative syndrome, cognitive syndrome, positive syndrome, and depression. Mean age of illness onset was 30.50 (±9.53) and

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mean duration of illness was 9.31 (±6.93) years. All patients were taking atypical antipsychotic medication. Seventeen age-matched (nine male) right-handed healthy control participants were also recruited as a comparison group. Healthy participants were only included if they had no history of psychiatric illness, no neurological injury, and no deficits in motor functioning. The study was approved by the local ethics committee, was performed in accordance with the Declaration of Helsinki, and all participants gave written consent to participate in the study. Table 1 shows demographics, symptoms, and self-report ratings for both groups, as well as results of group comparisons.

Action observation task design and stimuli For the action observation EEG task, video clips were shown to participants in which they saw two people (performers) sitting facing each other at a table, transferring coins from one bowl to one of three other bowls in the middle of the table. One of the three bowls was labeled with a “+” (reward), one with a “–” (punishment), and one with a “0” (neutral). Actions were seen either being performed from a first-person or third-person point of view, which were rewarding, punishing, or neutral (i.e., 2 × 3 design). The task structure is depicted in Figure 1, which follows the same design as in Brown et al. (2013). A total of 120 videos were presented in each testing session, in a pseudorandom order. Trials were split into six blocks, with a single video used in each trial and each video lasted for a total of 10 s. A block of eight practice trials came before the six blocks of main

TABLE 1 Demographics, symptoms, and self-report ratings

Sex (M/F) Age (SD) PANSS Positive (SD) Negative (SD) General (SD) IRI Fantasy scale (SD) Perspective-taking (SD) Empathic concern (SD) Personal distress (SD) UOT (SD) Tap mean (SD)

Healthy controls (N = 17)

Schizophrenia (N = 17)

Test statistic

9/8 38.29 (12.10)

9/8 41.71 (10.98)

– – –

19.13 (7.03) 24.93 (7.94) 45.40 (14.37)

– – –

13.25 (3.99) 15.81 (2.23) 14.94 (2.35) 7.88 (3.22) 16.18 (2.46) 143.38 (20.12)

12.81 (3.99) 14.94 (3.21) 15.31 (3.53) 11.00 (3.71) 11.12 (3.25) 119.79 (13.15)

F(1,33) F(1,33) F(1,33) F(1,33) F(1,33) F(1,33)

– t(33) = 0.86

= = = = = =

0.20 0.58 0.01 6.94 21.94 11.57

Notes: PANSS, Positive and Negative Syndrome Scale; IRI, Interpersonal Reactivity Index; UOT, Unexpected Outcomes Test.

p

.40

.66 .45 .91 .01

Reward modulates the mirror neuron system in schizophrenia: A study into the mu rhythm suppression, empathy, and mental state attribution.

Impairments in the mirror neuron system (MNS) have been implicated as a possible underlying neurological basis for deficits in higher-level social cog...
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