Brain Advance Access originally published online on December 7, 2009
Brain 2010 133(1):262-271; doi:10.1093/brain/awp291
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Misattributions of agency in schizophrenia are based on imprecise predictions about the sensory consequences of one's actions
1 Department of Cognitive Neurology, Hertie-Institute for Clinical Brain Research, University of Tübingen, 72076 Tübingen, Germany 2 Department of Neurodegeneration, Hertie-Institute for Clinical Brain Research, University of Tübingen, 72076 Tübingen, Germany 3 Department of Psychiatry, University Hospital Marburg, Rudolf-Bultmann-Straße 8, 35039 Marburg, Germany 4 Department of Psychiatry, University Hospital Tübingen, Osianderstraße 24, 72076 Tübingen, Germany
Correspondence to: Matthis Synofzik, Department of Neurodegeneration, Hertie-Institute for Clinical Brain Research, Hoppe-Seyler-Straße 3, 72076 Tübingen, Germany E-mail: matthis.synofzik{at}uni-tuebingen.de
Correspondence may also be addressed to: Axel Lindner, Department of Cognitive Neurology, Hertie-Institute for Clinical Brain Research, Hoppe-Seyler-Straße 3, 72076 Tübingen, Germany E-mail: a.lindner{at}medizin.uni-tuebingen.de
The experience of being the initiator of one's own actions seems to be infallible at first glance. Misattributions of agency of one's actions in certain neurological or psychiatric patients reveal, however, that the central mechanisms underlying this experience can go astray. In particular, delusions of influence in schizophrenia might result from deficits in an inferential mechanism that allows distinguishing whether or not a sensory event has been self-produced. This distinction is made by comparing the actual sensory information with the consequences of one's action as predicted on the basis of internal action-related signals such as efference copies. If this internal prediction matches the actual sensory event, an action is registered as self-caused; in case of a mismatch, the difference is interpreted as externally produced. We tested the hypothesis that delusions of influence are based on deficits in this comparator mechanism. In particular, we tested whether patients’ impairments in action attribution tasks are caused by imprecise predictions about the sensory consequences of self-action. Schizophrenia patients and matched controls performed pointing movements in a virtual-reality setup in which the visual consequences of movements could be rotated with respect to the actual movement. Experiment 1 revealed higher thresholds for detecting experimental feedback rotations in the patient group. The size of these thresholds correlated positively with patients’ delusions of influence. Experiment 2 required subjects to estimate their direction of pointing visually in the presence of constantly rotated visual feedback. When compared to controls, patients’ estimates were significantly better adapted to the feedback rotation and exhibited an increased variability. In interleaved trials without visual feedback, i.e. when pointing estimates relied solely on internal action-related signals, this variability was likewise increased and correlated with both delusions of influence and the size of patients’ detection thresholds as assessed in the first experiment. These findings support the notion that delusions of influence are based on imprecise internal predictions about the sensory consequences of one's actions. Moreover, we suggest that such imprecise predictions prompt patients to rely more strongly on (and thus adapt to) external agency cues, in this case vision. Such context-dependent weighted integration of imprecise internal predictions and alternative agency cues might thus reflect the common basis for the various misattributions of agency in schizophrenia patients.
Key Words: agency; schizophrenia; efference copy; self; perception; optimal cue integration; Bayes
Abbreviations: PD, pointing direction; SAPS, Scale for the Assessment of Positive Symptoms
Received June 6, 2009. Revised September 5, 2009. Accepted September 26, 2009.