Association of impaired EEG mu wave suppression, negative symptoms and social functioning in biological motion processing in first episode of psychosis

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Abstract

Background

Event related desynchronization (ERD) of mu waves, or mu suppression, over sensorimotor cortex has been observed in response to self-generated movement, viewing movement, or imaging movement. Mu suppression is especially pronounced when the movement has social relevance and is being generated by a biological entity indicating successful social adaptation. And since social adaptation problems are common in schizophrenia, the authors designed a study to test mu wave suppression in a first episode of psychosis population.

Methods

A total of 32 subjects (first episode of psychosis patients N = 20; healthy comparison subjects N = 12) aged 13–34 watched movement videos with and without socially relevant cues, executed by biological or non-biological agents. Scalp electrode EEG recordings of mu rhythm (8–13 Hz) over sensorimotor cortex during the session were used to calculate mu wave suppression. Average mu suppression was compared within and between groups, as well as correlations between mu suppression and clinical measures.

Results

First episode patients showed significantly reduced mu wave suppression over sensorimotor cortex when viewing biological motion, compared to healthy subjects. In addition, negative symptom burden and poor social adjustment correlated with impaired mu wave suppression.

Conclusions

Our finding provides the first description of impaired event related desynchronization of mu waves in response to biological motion and its correlation with negative symptoms and social adjustment in the first episode of psychosis. Future studies can be conducted to determine if mu wave suppression represents an endophenotype with potential applications in biological treatments of negative symptoms and social functioning deficits in schizophrenia.

Introduction

The mu rhythm is an EEG oscillation in the 8–13 Hz band, detected over sensorimotor cortex. Large amplitude, synchronous mu waves found at rest, transition to smaller amplitude desynchronous waves when a subject performs a motor activity (Gastaut, 1952, Pineda, 2005). This phenomenon of event related desynchronization (ERD) or “mu wave suppression” is also observed when a subject watches someone else perform an action (Muthukumaraswamy et al., 2004), or imagines an action being performed (Pfurtscheller et al., 2006). Additional studies suggest that mu oscillations are especially responsive to motor activity in a social context originating from a biological agent rather than an inanimate object (Oberman et al., 2007). Experiments involving typical participants have linked EEG mu suppression to higher order social information processing (Oberman et al., 2007), theory of mind (Pineda and Hecht, 2009, Perry et al., 2010), and empathy (Cheng et al., 2008a, Cheng et al., 2008b), implying a connection between mu suppression and social adaptation. In addition, studies in autism, a disorder with striking social deficits, have demonstrated reduced mu wave suppression in autistic children with otherwise normal intelligence (Martineau et al., 2004, Oberman et al., 2005, Ramachandran and Oberman, 2006).

Taken together, these findings suggest that mu wave suppression measures the workings of a neural network integral to the processing of socially adaptive environmental stimuli. It is plausible that aberrant network processing may be present in other psychiatric disorders with social deficits, not just autism, thereby representing a common pathway for impaired social adaptation.

To test this hypothesis, we designed a study assessing mu wave suppression in subjects in a first episode of psychosis (FE) in response to observation of socially relevant movement videos originating from biological agents. Since schizophrenia is a neuro-developmental disorder, studying early stages of psychosis could provide insights into the pathogenesis of the disorder, with implications for treatment and prevention.

Section snippets

Subjects

All subjects, 20 FE and 12 normal controls (NC) provided consent for the study (IRB#090383). This project was reviewed and approved by the UCSD Human Research Protections Program. FE subjects were recruited as part of the Cognitive Assessment and Risk Evaluation (CARE) program based in the UCSD Outpatient Psychiatric services clinic. The program is well known in the San Diego area and receives referrals from community clinics, local schools and private psychiatrists. Control subjects were

Results

In order to investigate group differences in mu suppression, a repeated measures analysis of variance (ANOVA) with condition (moving human hand, social interaction, and biological motion) and electrode site (C3, Cz, and C4) as the within-subject variables and diagnostic group (NC and FE) as the between-subject variable was performed. Since age was significantly different between the two groups, age was used as a covariate for comparisons between the two groups.

Discussion

This is the first study of event related desynchronization (ERD) of mu rhythm over sensorimotor cortex in individuals experiencing a first episode of psychosis. Compared to typically developing individuals, first episode subjects showed similar mu wave suppression when viewing 1) a moving human hand and 2) a social interaction depicted by a game of catch. FE subjects showed significantly lower mu wave suppression when viewing biological motion in a point light display animation video.

Point

Role of funding source

Funding for this study was provided by the Mental Illness Research, Education and Clinical Center (MIRECC) program, Academic Senate Grant from the University of California at San Diego and the National Institute of Mental Health (R01 MH060720, K24 MH076191, and MH076191). The MIRECC, Academic Senate and NIMH had no further role in study design; in the collection, analysis and interpretation of data; in writing the report; and in the decision to submit the paper for publication.

Contributors

Dr. Singh carried out the testing, analyzed the data and wrote the manuscript. Dr. Pineda provided mentorship in study design, data analysis and editing of the manuscript. Dr. Cadenhead provided mentorship in study design, data analysis and editing of the manuscript. All authors contributed to and have approved the final manuscript.

Conflict of interest

All authors declare that they have no conflicts of interest.

Acknowledgments

The authors thank Jason Nunag for technical support, Kathleen Shafer for IRB related issues and Dr. Shahrukh Golshan for his help with statistical analyses.

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