Abstract

The syndrome of anosognosia for hemiplegia, or the lack of awareness for one’s paralysis following right hemisphere stroke, can provide unique insights into the neurocognitive mechanisms of self-awareness. Yet it remains unclear whether anosognosia for hemiplegia is a modality-specific deficit of sensorimotor monitoring, or whether domain-general processes of attention and belief-updating converge to cause anosognosia for hemiplegia. Using a Bayesian learning framework, we formalized and empirically investigated the hypothesis that failures to update anosognosic beliefs can be explained by abnormalities in the relative uncertainty (i.e. precision) ascribed to prior beliefs versus sensory information in different contexts. We designed a new motor belief-updating task that manipulated both the temporal (prospective and retrospective) and spatial (hemispace most affected by inattention and hemispace less affected by inattention) conditions in which beliefs had to be updated, and we validated its sensitivity to anosognosia for hemiplegia in 26 patients with right hemisphere stroke. We then computed and empirically tested two different Bayesian predictors of prospective beliefs using two proxies for precision in anosognosia for hemiplegia patients: (i) standardized, neuropsychological measures of objective attention abilities, i.e. visuospatial neglect scores and (ii) subjective uncertainty reports, i.e. confidence ratings. Our results suggest that while neglect does not affect local, sensorimotor error monitoring, it does seem to affect the degree to which observed errors are used to update more general, prospective beliefs about counterfactual motor abilities in anosognosia for hemiplegia. Difficulties in such ‘counterfactual’ belief-updating were associated with disruptions in tracts of the ventral attentional network (i.e. superior longitudinal fasciculus connecting the temporo-parietal junction and ventral frontal cortex) and associated lesions to the insula, inferior parietal cortex and superior temporal regions. These results suggest that self-awareness extends beyond local, retrospective monitoring, requiring also salience-based, convergence of beliefs about the self that go beyond the ‘here-and-now’ of sensorimotor experience.

Highlights

  • In order to navigate a changing world, people have to update their current beliefs in the face of new evidence

  • We hypothesized that anosognosia for hemiplegia (AHP) patients would have greater difficulties in monitoring their errors retrospectively and updating their beliefs prospectively in the affected than the unaffected hemispace, where their inattention would render prediction errors imprecise and would influence the relative precision of prior beliefs and sensory prediction errors

  • We attempted to address outstanding questions regarding the inability of patients with AHP to update their beliefs about their motor abilities, despite the severe disabilities caused by stroke

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Summary

Introduction

In order to navigate a changing world, people have to update their current beliefs in the face of new evidence. This belief-updating may be facilitated by the monitoring and evaluation of experience, as when one notices one’s mistakes without any feedback. This ability is typically referred to as metacognition.[1,2] People may have different degrees of confidence (subjective uncertainty) about the accuracy of their perceptions or memories—and a large body of scientific evidence is dedicated to such ‘retrospective’ aspects of metacognition.[3] People may vary in how they metacognitively evaluate their abilities in the future. Metacognitive beliefs are an important part of the construct of metacognition, we can note that the terminology encompasses other processes as well (e.g. there are ongoing debates about the precise relation between metamemory and mentalisation to perceptual metacognition)

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