Differential processing of metacognitive evaluation and the neural circuitry of the self and others in schizophrenia: A pilot study

BACKGROUND Impaired awareness of the self and others (i.e., metacognitive evaluations) are seen in schizophrenia. We compared patterns of activation in schizophrenia (SZ) and nonclinical subjects during a functional magnetic resonance imaging (fMRI) task of metacognitive evaluations that has been demonstrated to engage the neural circuitry of the self in healthy subjects. METHODS Eleven SZ subjects (7 males, mean age 26.6+/-8) and 10 healthy control subjects (4 males, mean age 29.6+/-8.4) were enrolled. Participants completed two runs of a metacognitive evaluation task (self vs. other vs. word meaning). fMRI data was obtained using a full body Bruker MedSped 4.0Tesla system. Group contrasts were performed using an uncorrected p<0.005 with a 50voxel extent threshold. RESULTS We observed a significant hypoactivation in the left superior temporal sulcus (STS) during metacognitive evaluations of others (OE) vs. semantic positivity evaluations (SPE) and a trend toward significant hypoactivation in the OE vs. self evaluations (SE) in the SZ group. Significant hypoactivation was also seen in the right inferior temporal gyrus (ITG) in the OE vs. SE contrasts in the SZ group. A trendworthy hypoactivation was seen in the SZ group in the right middle frontal gyrus and pole of the left STS during OE vs. SPE and SE contrasts respectively. CONCLUSIONS These results extend previous findings of impaired metacognitive evaluative processes in schizophrenia to aberrations of the neural circuitry implicated in self/other awareness among SZ patients. Greater understanding of the neural basis of deficits of self/other awareness in early schizophrenia may contribute to improvements in the identification and treatment of individuals at risk for the illness.

[1]  A. David,et al.  The self in neuroscience and psychiatry , 2003 .

[2]  ChrisD . Frith The Cognitive Neuropsychology of Schizophrenia , 1992 .

[3]  F. Happé Theory of Mind and the Self , 2003, Annals of the New York Academy of Sciences.

[4]  D C Rubin,et al.  Predicting which words get recalled: Measures of free recall, availability, goodness, emotionality, and pronunciability for 925 nouns , 1986, Memory & cognition.

[5]  J. Parnas,et al.  Phenomenology of anomalous self-experience in early schizophrenia. , 2003, Comprehensive psychiatry.

[6]  J. McEvoy,et al.  Source-monitoring deficits for self-generated stimuli in schizophrenia: multinomial modeling of data from three sources , 2002, Schizophrenia Research.

[7]  D. Stuss,et al.  The frontal lobes are necessary for 'theory of mind'. , 2001, Brain : a journal of neurology.

[8]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[9]  Rebecca Saxe,et al.  Overlapping and non-overlapping brain regions for theory of mind and self reflection in individual subjects. , 2006, Social cognitive and affective neuroscience.

[10]  J. Decety,et al.  Social brain dysfunctions in schizophrenia: A review of neuroimaging studies , 2006, Psychiatry Research: Neuroimaging.

[11]  Sterling C. Johnson,et al.  Metacognitive evaluation, self-relevance, and the right prefrontal cortex , 2004, NeuroImage.

[12]  Robert T. Schultz,et al.  Self, mother and abstract other: An fMRI study of reflective social processing , 2008, NeuroImage.

[13]  Thomas E. Nichols,et al.  Estimation efficiency and statistical power in arterial spin labeling fMRI , 2006, NeuroImage.

[14]  L. Sass The Self in Neuroscience and Psychiatry: Self-disturbance in schizophrenia: hyperreflexivity and diminished self-affection , 2003 .

[15]  M. Jeannerod,et al.  Neural correlates of action attribution in schizophrenia , 2004, Psychiatry Research: Neuroimaging.

[16]  N. Allen,et al.  Impaired theory of mind in first-episode schizophrenia: comparison with community, university and depressed controls , 2008, Schizophrenia Research.

[17]  G. Dimaggio,et al.  Metacognition amidst narratives of self and illness in schizophrenia: associations with neurocognition, symptoms, insight and quality of life , 2005, Acta psychiatrica Scandinavica.

[18]  Kevin A. Pelphrey,et al.  Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders , 2008, Schizophrenia Research.

[19]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  E. Bora,et al.  Theory of mind and unawareness of illness in schizophrenia , 2007, European Archives of Psychiatry and Clinical Neuroscience.

[21]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[22]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[23]  K. Vogeley The Self in Neuroscience and Psychiatry: Schizophrenia as disturbance of the self-construct , 2003 .

[24]  L. Seidman,et al.  The neuropsychological basis of insight in first-episode schizophrenia: a pilot metacognitive study , 2004, Schizophrenia Research.

[25]  W. Kintsch,et al.  Memory and cognition , 1977 .

[26]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[27]  Josef Parnas,et al.  Schizophrenia, consciousness, and the self. , 2003, Schizophrenia bulletin.

[28]  K. Zilles,et al.  Mind Reading: Neural Mechanisms of Theory of Mind and Self-Perspective , 2001, NeuroImage.

[29]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

[30]  Sterling C. Johnson,et al.  Neural correlates of self-reflection. , 2002, Brain : a journal of neurology.

[31]  Morris Goldsmith,et al.  Real-world cognitive--and metacognitive--dysfunction in schizophrenia: a new approach for measuring (and remediating) more "right stuff". , 2006, Schizophrenia bulletin.

[32]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[33]  Steven M. Platek,et al.  Neural correlates of self-face recognition: An effect-location meta-analysis , 2008, Brain Research.

[34]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[35]  Peter Thier,et al.  The posterior superior temporal sulcus is involved in social communication not specific for the eyes , 2008, Neuropsychologia.

[36]  J. Lieberman,et al.  Antipsychotic drug effects on brain morphology in first-episode psychosis. , 2005, Archives of general psychiatry.

[37]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.