Functional Magnetic Resonance Imaging of Impaired Sensory Prediction in Schizophrenia

Sukhwinder S. Shergill*, Thomas P. White, Daniel W. Joyce, Paul M. Bays, Daniel M. Wolpert, Chris D. Frith

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

124 Citations (Scopus)

Abstract

IMPORTANCE Forward models predict the sensory consequences of planned actions and permit discrimination of self-and non-self-elicited sensation; their impairment in schizophrenia is implied by an abnormality in behavioral force-matching and the flawed agency judgments characteristic of positive symptoms, including auditory hallucinations and delusions of control.

OBJECTIVE To assess attenuation of sensory processing by self-action in individuals with schizophrenia and its relation to current symptom severity.

DESIGN, SETTING, AND PARTICIPANTS Functional magnetic resonance imaging data were acquired while medicated individuals with schizophrenia (n = 19) and matched controls (n = 19) performed a factorially designed sensorimotor task in which the occurrence and relative timing of action and sensation were manipulated. The study took place at the neuroimaging research unit at the Institute of Cognitive Neuroscience, University College London, and the Maudsley Hospital.

RESULTS In controls, a region of secondary somatosensory cortex exhibited attenuated activation when sensation and action were synchronous compared with when the former occurred after an unexpected delay or alone. By contrast, reduced attenuation was observed in the schizophrenia group, suggesting that these individuals were unable to predict the sensory consequences of their own actions. Furthermore, failure to attenuate secondary somatosensory cortex processing was predicted by current hallucinatory severity.

CONCLUSIONS AND RELEVANCE Although comparably reduced attenuation has been reported in the verbal domain, this work implies that a more general physiologic deficit underlies positive symptoms of schizophrenia.

Original languageEnglish
Pages (from-to)28-35
Number of pages8
JournalJAMA Psychiatry
Volume71
Issue number1
DOIs
Publication statusPublished - 1 Jan 2014

Keywords

  • COROLLARY DISCHARGE
  • CONSEQUENCES
  • AGENCY
  • CHLORPROMAZINE
  • MODULATION
  • DISORDERS
  • FEEDBACK
  • DEFICITS
  • SPEECH

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