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

Tomassini, Alessandro; Cope, Thomas E; Zhang, Jiaxiang; Rowe, James B

doi:10.1093/braincomms/fcae065

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

Alessandro Tomassini

, Thomas E Cope, Jiaxiang Zhang

, James B Rowe

Brain Communications, Volume: 6, Issue: 2

Swansea University Author: Jiaxiang Zhang

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DOI (Published version): 10.1093/braincomms/fcae065

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
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URI:	https://cronfa.swan.ac.uk/Record/cronfa66058
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first_indexed	2024-04-15T12:32:14Z
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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. 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spelling	v2 66058 2024-04-15 Parkinson’s disease impairs cortical sensori-motor decision-making cascades 555e06e0ed9a87608f2d035b3bde3a87 0000-0002-4758-0394 Jiaxiang Zhang Jiaxiang Zhang true false 2024-04-15 MACS 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. Journal Article Brain Communications 6 2 Oxford University Press (OUP) 2632-1297 Parkinson’s disease, accumulator, uncertainty, visuomotor, decision-making 19 3 2024 2024-03-19 10.1093/braincomms/fcae065 COLLEGE NANME Mathematics and Computer Science School COLLEGE CODE MACS Swansea University Another institution paid the OA fee 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). 2024-05-22T12:03:32.8780438 2024-04-15T13:26:14.0213985 Faculty of Science and Engineering School of Mathematics and Computer Science - Computer Science Alessandro Tomassini 0000-0001-5645-6910 1 Thomas E Cope 2 Jiaxiang Zhang 0000-0002-4758-0394 3 James B Rowe 0000-0001-7216-8679 4 66058__30430__d0e6ff22c0664f52ad5edf815793899c.pdf 66058.VoR.pdf 2024-05-22T12:01:39.3535448 Output 1788863 application/pdf Version of Record true © The Author(s) 2024. This is an Open Access article distributed under the terms of the Creative Commons Attribution License. true eng https://creativecommons.org/licenses/by/4.0/
title	Parkinson’s disease impairs cortical sensori-motor decision-making cascades
spellingShingle	Parkinson’s disease impairs cortical sensori-motor decision-making cascades Jiaxiang Zhang
title_short	Parkinson’s disease impairs cortical sensori-motor decision-making cascades
title_full	Parkinson’s disease impairs cortical sensori-motor decision-making cascades
title_fullStr	Parkinson’s disease impairs cortical sensori-motor decision-making cascades
title_full_unstemmed	Parkinson’s disease impairs cortical sensori-motor decision-making cascades
title_sort	Parkinson’s disease impairs cortical sensori-motor decision-making cascades
author_id_str_mv	555e06e0ed9a87608f2d035b3bde3a87
author_id_fullname_str_mv	555e06e0ed9a87608f2d035b3bde3a87_***_Jiaxiang Zhang
author	Jiaxiang Zhang
author2	Alessandro Tomassini Thomas E Cope Jiaxiang Zhang James B Rowe
format	Journal article
container_title	Brain Communications
container_volume	6
container_issue	2
publishDate	2024
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issn	2632-1297
doi_str_mv	10.1093/braincomms/fcae065
publisher	Oxford University Press (OUP)
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description	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.
published_date	2024-03-19T12:03:31Z
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Parkinson’s disease impairs cortical sensori-motor decision-making cascades

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