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Original Investigation |

Functional Magnetic Resonance Imaging of Impaired Sensory Prediction in Schizophrenia

Sukhwinder S. Shergill, BSc, PhD, MBBCh, FRCPsych1; Thomas P. White, PhD1; Daniel W. Joyce, PhD1; Paul M. Bays, PhD2; Daniel M. Wolpert, PhD3; Chris D. Frith, FRS, FmedSci, FBA4
[+] Author Affiliations
1Department of Psychosis Studies, Institute of Psychiatry, King’s College London, London, United Kingdom
2Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, London, United Kingdom
3Sensorimotor Learning Group, Department of Engineering, University of Cambridge, Cambridge, United Kingdom
4Wellcome Trust Centre for Neuroimaging, University College London, London, United Kingdom
JAMA Psychiatry. 2014;71(1):28-35. doi:10.1001/jamapsychiatry.2013.2974.
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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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Figure 1.
The Experimental Setup

Force is applied to an upper sensor by the index finger on the right hand (RH) and transmitted to the index finger on the left hand (LH) via a sensor mounted on a lever driven by a torque motor. Computerized control of this system manipulated the occurrence and timing of left index finger sensations in both the absence and presence of right index finger movements.

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Figure 2.
Significant Main Effects of Motion, Sensation, and Group

A-C, Motor effects according to the red F-value scale. D-F, Sensation effects according to the orange F-value scale. G-I, Group effects according to the blue F-value scale. Images are overlaid on a standard T1-weighted magnetic resonance image and shown according to the neurologic convention.

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Figure 3.
Condition-Specific Task Estimates and Region of Interest Location

A, Primary somatosensory cortex; B, secondary somatosensory cortex; C, cerebellum. Error bars indicate SEM. M1S1D0 indicates force transmitted synchronously; M1S1D1, force transmitted with delay; and M0S1D0, force transmitted without movement.

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Figure 4.
Sensory Attenuation in Secondary Somatosensory Cortex and Current Hallucinatory Severity as Measured Using the Positive and Negative Syndrome Scale24

Individual-specific data for the schizophrenia group and the associated best-fit line are shown (R2 linear = .214).

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