Embodied Predictions, Agency, and Psychosis

Abstract

Psychotic symptoms, i.e., hallucinations and delusions, involve gross departures from conscious apprehension of consensual reality; respectively, perceiving and believing things that, according to same culture peers, do not obtain. In schizophrenia, those experiences are often related to abnormal sense of control over one's own actions, often expressed as a distorted sense of agency (i.e., passivity symptoms). Cognitive and computational neuroscience have furnished an account of these experiences and beliefs in terms of the brain's generative model of the world, which underwrites inferences to the best explanation of current and future states, in order to behave adaptively. Inference then involves a reliability-based trade off of predictions and prediction errors, and psychotic symptoms may arise as departures from this inference process, either an over-or under-weighting of priors relative to prediction errors. Surprisingly, there is empirical evidence in favor of both positions. Relatedly, there is evidence for both an enhanced and a diminished sense of agency in schizophrenia. How can this be? We argue that there is more than one generative model in the brain, and that ego-and allo-centric models operate in tandem. In brief, ego-centric models implement corollary discharge signals that cancel out the effects of self-generated actions while allo-centric models compare several hypothesis regarding the causes of sensory inputs (including the self among the potential causes). The two parallel hierarchies give rise to different levels of agency, with ego-centric models subserving "feelings of agency" and allo-centric predictions giving rise to "judgements of agency." Those two components are weighted according to their reliability and combined, generating a higher-level "sense of agency." We suggest that in schizophrenia a failure of corollary discharges to suppress self-generated inputs results in the absence of a "feeling of agency" and in a compensatory enhancement of allo-centric priors, which might underlie hallucinations, delusions of control but also, under certain circumstances, the enhancement of "judgments of agency." We discuss the consequences of such a model, and potential courses of action that could lead to its falsification.

Relating glutamate, conditioned, and clinical hallucinations via 1H-MR Spectroscopy

“…Instead, we only observed a negative correlation between insular Glx and 𝜈, which is compatible with high-level prediction errors being driven either by within-insula aberrant prediction errors, likely tethered to neuromodulators (dopamine, acetylcholine or serotonin) 2 or by abnormalities in a parallel hierarchy, e.g. weak egocentric corollary discharge signals 40 . For instance, low glutamate concentration might be the result of excessive striatal dopamine release, which has also been linked to overreliance on prior expectations 41 and increased detection of missing tones in a conditioned hallucinations task 5 .…”

Impaired Sense of Agency and Associated Confidence in Psychosis

“…that the over-attribution bias may originate from more explicit top-down processes that take into account intentions, beliefs and contextual information in forming judgments of agency that compensate for the lack of sensorimotor signals that typically form the basis for SoA (Synofzik et al, 2008(Synofzik et al, , 2009. Indeed, reduced precision of sensorimotor predictive models may lead to overweighting top-down priors, causing an overattribution of SoA to the Self (Corlett et al, 2019;Leptourgos & Corlett, 2020). Our current finding of high subjective ratings of confidence despite low accuracy of SoA performance (i.e., impaired metacognition), support this hypothesis that top-down explicit processes (i.e., 'I moved and saw a movement so it is likely me') may receive higher weightings despite impairments in sensorimotor prediction function in psychosis.…”

“…Disturbances of SoA are a striking aspect of psychosis, common across schizophrenia spectrum disorders (Franck et al, 2001;Frith & Done, 1989;Haggard et al, 2003;Hauser et al, 2011;Maeda et al, 2012;Voss et al, 2010). It has been suggested that aberrant hierarchical prediction mechanisms underlie psychosis symptoms (Corlett et al, 2019;Fletcher & Frith, 2008;Sterzer et al, 2018) and specifically abnormal SoA (Frith & Done, 1989;Leptourgos & Corlett, 2020). Accordingly, psychosis patients exhibit reduced sensory and neural attenuation for actions (Ford et al, 2013;Shergill et al, 2005Shergill et al, , 2014, impaired ability to predict the outcomes of their actions (Lindner et al, 2005;Synofzik et al, 2010;Voss et al, 2010) and erroneous explicit judgments of agency (Fourneret et al, 2002;Franck et al, 2001).…”

“…While these paradigms have enriched our understanding of learned action outcome mechanisms, they do not tap into the strong predictive capacities afforded by a lifelong experience of controlling our bodies (Stern et al, 2020). Thus, embodied SoA may differ in regards to the strength of the priors of the predictive processes (Allen & Tsakiris, 2018;Leptourgos & Corlett, 2020), and better capture psychotic patients' anomalous self-experiences (Sass & Parnas, 2003).…”

The positive dimension of schizotypy is associated with a reduced attenuation and precision of self-generated touch

“…First, it enables the nervous system to detect situations that can be physically harmful for the organism and to act accordingly (Brooks and Cullen, 2019;Crapse and Sommer, 2008;McNamee and Wolpert, 2019): for example, the touch of a spider crawling up one's arm (externally generated touch) elicits a dramatically different response from the same touch applied by one's other hand (self-generated touch). Second, this distinction is a prerequisite for maintaining our self-consciousness and consequently our mental health because it allows us to delimit our own intentions, sensations, actions, thoughts and emotions from those of others and perceive ourselves as independent human entities (Blakemore and Frith, 2003;Frith, 2005a;Leptourgos and Corlett, 2020). For example, we do not mistake our thoughts for the voices of other people we simultaneously have conversation with because we attribute the cause of our thoughts to ourselves (self-generated 'voices') and the cause of the voices we hear to the other people (externally generated voices).…”