Functional magnetic resonance imaging of impaired sensory prediction in schizophrenia
Open accessAbstract
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.
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- Authors
- Shergill, S. S., White, T. P., Joyce, D. W., Bays, P. M., Wolpert, D. M., & Frith, C. D.
- Affiliations
- King's College London (GB)
- Department of Psychosis Studies, Institute of Psychiatry, King’s College London, London, United Kingdom
- UCL Queen Square Institute of Neurology (GB)
- University of Cambridge (GB)
- Wellcome Centre for Human Neuroimaging (GB)
- Corresponding author
- Shergill, Sukhwinder S.
- Venue
- JAMA Psychiatry
- Publisher
- American Medical Association (AMA)
- Published
- 2014-01-01
- Volume
- 71
- Issue
- 1
- Pages
- 28
- ISSN
- 2168-622X (ISSN-L)
- OpenAlex
- W2130309455
- Cited by
- 163
- References
- 40
- Citations by year
- 2026: 6 · 2025: 16 · 2024: 20 · 2023: 11 · 2022: 14 · 2021: 9 · 2020: 18 · 2019: 14 · 2018: 10 · 2017: 14 · 2016: 8 · 2015: 14 · 2014: 9
- FWCI
- 7.32
- Type
- journal article
- Language
- en
- Open access
- green
- kclpure.kcl.ac.uk
- Licence
- other-oa
- Locations
- JAMA Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (publishedVersion, other-oa)
- Cambridge University Engineering Department Publications Database (submittedVersion)
- Funders
- Wellcome Trust (091593, 097803, 097803/Z/11/Z)
- National Institute for Health and Care Research (ACF-2012-17-001)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Free Will and Agency
- Social Sciences › Arts and Humanities › Philosophy › Mental Health and Psychiatry
- Keywords
- schizophrenia, forward model, sensory prediction, self-action, secondary somatosensory cortex, sensorimotor tasks, auditory hallucinations, positive symptoms, delusions of control, force matching, symptom severity
- MeSH terms
- Adult, Cerebellum, Female, Hallucinations, Humans, Magnetic Resonance Imaging, Male, Psychomotor Performance, Schizophrenia, Sensation, Severity of Illness Index, Somatosensory Cortex, Case-Control Studies, Feedback, Sensory, Functional Neuroimaging
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