Misattributions of agency in schizophrenia are based on imprecise predictions about the sensory consequences of one's actions

Abstract

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.

Intentional binding and the sense of agency: A review

“…That is, the strength of outcome prediction was not related to the objective likelihood of the outcome and instead, predictions were equally strong in the high and low outcome probability conditions. Imprecise prediction has also been observed in a separate study using a different agency paradigm (Synofzik, Thier, Leube, Schlotterbeck, & Lindner, 2010). Imprecise sensorimotor prediction may explain the stronger retrospective contribution to intentional binding in patients: given unreliable internal sensorimotor predictions, the patients' experience of agency may be strongly influenced by the more reliable external cues to agency.…”

“…Importantly, it can explain patterns of agency experience associated with certain neurological and psychiatric diseases. For example, the sense of agency in patients with schizophrenia appears to be characterised by noisy sensorimotor prediction (Voss et al, 2010;Synofzik et al, 2010).…”

Judgements of agency in schizophrenia: an impairment in autonoetic metacognition

“…Jeannerod [5] and others [6,7] have noted that patients with positive symptoms of schizophrenia, such as hearing voices and experiencing hallucinations and delusions, have difficulty in accurately reflecting upon their own agency. Such symptoms are also related to imaging findings showing hyperactivity in areas of the brain, in particular, the temporal parietal junction [8], that relate to the detection of a discrepancy between one's own intentions and the outcome that ensues [9].…”

Physical and mental effort disrupts the implicit sense of agency

“…Several accounts as to how agency is attributed to the self have been suggested, including the forward predictive comparator model (Blakemore, Frith & Wolpert, 2001;Blakemore, Wolpert & Frith, 2002;Wegner, Sparrow, & Winerman, 2004), the post-hoc inference account (Wegner & Wheatley, 1999), and the optimal cue integration account (Moore & Fletcher, 2012;Synofzik, Thier, Leube, Schlotterbeck, & Lindner, 2010;Synofzik, Vosgerau, & Lindner, 2009;Synofzik, Vosgerau, & Voss, 2013). The comparator model provides a predictive account of agency attribution, characterised by the comparison between predicted action effects with actual action effects.…”