Parkinson’s disease impairs cortical sensori-motor decision-making cascades

Author:

Tomassini Alessandro1ORCID,Cope Thomas E123,Zhang Jiaxiang4ORCID,Rowe James B123ORCID

Affiliation:

1. MRC Cognition and Brain Sciences Unit, University of Cambridge 1 , Cambridge CB2 7EF , UK

2. Department of Clinical Neurosciences, University of Cambridge , Cambridge CB2 0SZ , UK

3. Department of Neurology, Cambridge University Hospitals NHS Trust , Cambridge CB2 0QQ , UK

4. Department of Computer Science, Swansea University , Swansea SA18EN , UK

Abstract

Abstract The transformation from perception to action requires a set of neuronal decisions about the nature of the percept, identification and selection of response options and execution of the appropriate motor response. The unfolding of such decisions is mediated by distributed representations of the decision variables—evidence and intentions—that are represented through oscillatory activity across the cortex. Here we combine magneto-electroencephalography and linear ballistic accumulator models of decision-making to reveal the impact of Parkinson’s disease during the selection and execution of action. We used a visuomotor task in which we independently manipulated uncertainty in sensory and action domains. A generative accumulator model was optimized to single-trial neurophysiological correlates of human behaviour, mapping the cortical oscillatory signatures of decision-making, and relating these to separate processes accumulating sensory evidence and selecting a motor action. We confirmed the role of widespread beta oscillatory activity in shaping the feed-forward cascade of evidence accumulation from resolution of sensory inputs to selection of appropriate responses. By contrasting the spatiotemporal dynamics of evidence accumulation in age-matched healthy controls and people with Parkinson’s disease, we identified disruption of the beta-mediated cascade of evidence accumulation as the hallmark of atypical decision-making in Parkinson’s disease. In frontal cortical regions, there was inefficient processing and transfer of perceptual information. Our findings emphasize the intimate connection between abnormal visuomotor function and pathological oscillatory activity in neurodegenerative disease. We propose that disruption of the oscillatory mechanisms governing fast and precise information exchanges between the sensory and motor systems contributes to behavioural changes in people with Parkinson’s disease.

Funder

Medical Research Council

Wellcome Trust

Cambridge University Centre for Parkinson-plus

National Institute for Health and Care Research Cambridge Biomedical Research Centre

National Institute for Health and Care Research

European Research Council

Publisher

Oxford University Press (OUP)

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