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Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose

Noham Wolpe Orcid Logo, Jiaxiang Zhang Orcid Logo, Cristina Nombela Orcid Logo, James N. Ingram Orcid Logo, Daniel M. Wolpert Orcid Logo, Cam-CAN, James B. Rowe Orcid Logo

Scientific Reports, Volume: 8, Issue: 1

Swansea University Author: Jiaxiang Zhang Orcid Logo

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DOI (Published version): 10.1038/s41598-018-33678-3

Abstract

Abnormal initiation and control of voluntary movements are among the principal manifestations of Parkinson’s disease (PD). However, the processes underlying these abnormalities and their potential remediation by dopamine treatment remain poorly understood. Normally, movements depend on the integrati...

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Published in: Scientific Reports
ISSN: 2045-2322
Published: Springer Science and Business Media LLC 2018
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URI: https://cronfa.swan.ac.uk/Record/cronfa61344
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This integration leads to a suppression in the intensity of predicted sensations, reflected in a &#x2018;sensory attenuation&#x2019;. We examined this integration process and its relation to dopamine in PD, by measuring sensory attenuation. Patients with idiopathic PD (n = 18) and population-derived controls (n = 175) matched a set of target forces applied to their left index finger by a torque motor. To match the force, participants either pressed with their right index finger (&#x2018;Direct&#x2019; condition) or moved a knob that controlled a motor through a linear potentiometer (&#x2018;Slider&#x2019; condition). We found that despite changes in sensitivity to different forces, overall sensory attenuation did not differ between medicated PD patients and controls. Importantly, the degree of attenuation was negatively related to PD motor severity but positively related to individual patient dopamine dose, as measured by levodopa dose equivalent. 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McDonnell Foundation 21st Century Science Initiative: Scholar Award in Understanding Human Cognition. NW was funded by Gates Cambridge. DMW received grants from the Wellcome Trust (097803), Human Frontier Science Program and the Royal Society Noreen Murray Professorship in Neurobiology. Cam-CAN was supported by the Biotechnology and Biological Sciences Research Council (BB/H008217/1). 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spelling 2022-10-11T12:31:10.4833350 v2 61344 2022-09-26 Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose 555e06e0ed9a87608f2d035b3bde3a87 0000-0002-4758-0394 Jiaxiang Zhang Jiaxiang Zhang true false 2022-09-26 SCS Abnormal initiation and control of voluntary movements are among the principal manifestations of Parkinson’s disease (PD). However, the processes underlying these abnormalities and their potential remediation by dopamine treatment remain poorly understood. Normally, movements depend on the integration of sensory information with the predicted consequences of action. This integration leads to a suppression in the intensity of predicted sensations, reflected in a ‘sensory attenuation’. We examined this integration process and its relation to dopamine in PD, by measuring sensory attenuation. Patients with idiopathic PD (n = 18) and population-derived controls (n = 175) matched a set of target forces applied to their left index finger by a torque motor. To match the force, participants either pressed with their right index finger (‘Direct’ condition) or moved a knob that controlled a motor through a linear potentiometer (‘Slider’ condition). We found that despite changes in sensitivity to different forces, overall sensory attenuation did not differ between medicated PD patients and controls. Importantly, the degree of attenuation was negatively related to PD motor severity but positively related to individual patient dopamine dose, as measured by levodopa dose equivalent. The results suggest that dopamine could regulate the integration of sensorimotor prediction with sensory information to facilitate the control of voluntary movements. Journal Article Scientific Reports 8 1 Springer Science and Business Media LLC 2045-2322 Sensory Attenuation; Dose Dopamine; Target Force; Sensorimotor Prediction; Levodopa Equivalent Dose (LDE) 23 10 2018 2018-10-23 10.1038/s41598-018-33678-3 COLLEGE NANME Computer Science COLLEGE CODE SCS Swansea University The study was funded by grants to JBR from the Wellcome Trust (103838), Medical Research Council (SUAG/004 RG91365) and James S. McDonnell Foundation 21st Century Science Initiative: Scholar Award in Understanding Human Cognition. NW was funded by Gates Cambridge. DMW received grants from the Wellcome Trust (097803), Human Frontier Science Program and the Royal Society Noreen Murray Professorship in Neurobiology. Cam-CAN was supported by the Biotechnology and Biological Sciences Research Council (BB/H008217/1). JZ was funded by the European Research Council Starting Grant (716321). 2022-10-11T12:31:10.4833350 2022-09-26T11:37:41.2343340 Faculty of Science and Engineering School of Mathematics and Computer Science - Computer Science Noham Wolpe 0000-0002-4652-7727 1 Jiaxiang Zhang 0000-0002-4758-0394 2 Cristina Nombela 0000-0002-9806-2351 3 James N. Ingram 0000-0003-2567-504x 4 Daniel M. Wolpert 0000-0003-2011-2790 5 Cam-CAN 6 James B. Rowe 0000-0001-7216-8679 7 61344__25407__0b0930fa61a44db898a52766b58a6e9f.pdf 61344_VoR.pdf 2022-10-11T12:30:00.1502658 Output 1464475 application/pdf Version of Record true This article is licensed under a Creative Commons Attribution 4.0 International License true eng http://creativecommons.org/licenses/by/4.0/
title Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose
spellingShingle Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose
Jiaxiang Zhang
title_short Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose
title_full Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose
title_fullStr Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose
title_full_unstemmed Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose
title_sort Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose
author_id_str_mv 555e06e0ed9a87608f2d035b3bde3a87
author_id_fullname_str_mv 555e06e0ed9a87608f2d035b3bde3a87_***_Jiaxiang Zhang
author Jiaxiang Zhang
author2 Noham Wolpe
Jiaxiang Zhang
Cristina Nombela
James N. Ingram
Daniel M. Wolpert
Cam-CAN
James B. Rowe
format Journal article
container_title Scientific Reports
container_volume 8
container_issue 1
publishDate 2018
institution Swansea University
issn 2045-2322
doi_str_mv 10.1038/s41598-018-33678-3
publisher Springer Science and Business Media LLC
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Mathematics and Computer Science - Computer Science{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Mathematics and Computer Science - Computer Science
document_store_str 1
active_str 0
description Abnormal initiation and control of voluntary movements are among the principal manifestations of Parkinson’s disease (PD). However, the processes underlying these abnormalities and their potential remediation by dopamine treatment remain poorly understood. Normally, movements depend on the integration of sensory information with the predicted consequences of action. This integration leads to a suppression in the intensity of predicted sensations, reflected in a ‘sensory attenuation’. We examined this integration process and its relation to dopamine in PD, by measuring sensory attenuation. Patients with idiopathic PD (n = 18) and population-derived controls (n = 175) matched a set of target forces applied to their left index finger by a torque motor. To match the force, participants either pressed with their right index finger (‘Direct’ condition) or moved a knob that controlled a motor through a linear potentiometer (‘Slider’ condition). We found that despite changes in sensitivity to different forces, overall sensory attenuation did not differ between medicated PD patients and controls. Importantly, the degree of attenuation was negatively related to PD motor severity but positively related to individual patient dopamine dose, as measured by levodopa dose equivalent. The results suggest that dopamine could regulate the integration of sensorimotor prediction with sensory information to facilitate the control of voluntary movements.
published_date 2018-10-23T04:20:07Z
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