Deficits in sensory prediction are related to delusional ideation in healthy individuals

Christoph Teufel,Arjun Kingdon,James N Ingram,Daniel M Wolpert,Paul C Fletcher

doi:10.1016/j.neuropsychologia.2010.10.024

Christoph Teufel, Arjun Kingdon + Show 3 more

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https://doi.org/10.1016/j.neuropsychologia.2010.10.024

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Journal: Neuropsychologia	Publication Date: Oct 23, 2010
Citations: 69	License type: cc-by

Affiliation: University of Cambridge

Abstract

Motor control strongly relies on neural processes that predict the sensory consequences of self-generated actions. Previous research has demonstrated deficits in such sensory-predictive processes in schizophrenic patients and these low-level deficits are thought to contribute to the emergence of delusions of control. Here, we examined the extent to which individual differences in sensory prediction are associated with a tendency towards delusional ideation in healthy participants. We used a force-matching task to quantify sensory-predictive processes, and administered questionnaires to assess schizotypy and delusion-like thinking. Individuals with higher levels of delusional ideation showed more accurate force matching suggesting that such thinking is associated with a reduced tendency to predict and attenuate the sensory consequences of self-generated actions. These results suggest that deficits in sensory prediction in schizophrenia are not simply consequences of the deluded state and are not related to neuroleptic medication. Rather they appear to be stable, trait-like characteristics of an individual, a finding that has important implications for our understanding of the neurocognitive basis of delusions.

Highlights

Predicting the sensory consequences of self-generated action is a key component of motor control (Wolpert & Flanagan, 2001)
Given that the Peters et al Delusion Inventory (PDI) and the Magical Ideation Scale (MgI) are both measures of delusional ideation, it is unsurprising that a partial correlation analysis controlled for handedness showed that their scores were significantly related to each other (r = .46, p ≤ .01), a finding consistent with previous studies (Peters et al, 1999)
In order to relate the questionnaires to sensory prediction, we calculated a composite score for each participant in the force-matching task by subtracting the average force applied in the Slider condition from that applied in the Finger condition

Summary

Introduction

Predicting the sensory consequences of self-generated action is a key component of motor control (Wolpert & Flanagan, 2001). Predictive attenuation explains why the tactile stimulation that we perceive when we Deficits in sensory-predictive processes have been linked to specific symptoms in psychopathology, most notably delusions of control in schizophrenic patients (Frith, Blakemore, & Wolpert, 2000; Lindner, Thier, Kircher, Haarmeier, & Leube, 2005; Shergill, Samson, Bays, Frith, & Wolpert, 2005; Synofzik, Thier, Leube, Schlotterbeck, & Lindner, 2010). Patients suffering from such delusions experience their own actions as being made for them by an external agent rather than by their own will. Persistence of prediction-error would lead to a reduced sense of agency, which is especially noteworthy given that many of the first-rank symptoms of schizophrenia seem to reflect external attributions of internally generated phenomena (Fletcher & Frith, 2009)

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