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

Alessandro Tomassini Orcid Logo, Thomas E Cope, Jiaxiang Zhang Orcid Logo, James B Rowe Orcid Logo

Brain Communications, Volume: 6, Issue: 2

Swansea University Author: Jiaxiang Zhang Orcid Logo

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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 decis...

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Published in: Brain Communications
ISSN: 2632-1297
Published: Oxford University Press (OUP) 2024
Online Access: Check full text

URI: https://cronfa.swan.ac.uk/Record/cronfa66058
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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.
Keywords: Parkinson’s disease, accumulator, uncertainty, visuomotor, decision-making
College: Faculty of Science and Engineering
Funders: This research was supported by the Medical Research Council (MC_UU_00030/14; MR/T033371/1), Wellcome Trust (103838; 220258), the Cambridge University Centre for Parkinson-plus and the National Institute for Health and Care Research (Cambridge Biomedical Research Centre, NIHR203312). T.E.C. was supported by the National Institute for Health and Care Research. J.Z. was supported by a European Research Council grant (716321).
Issue: 2