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

Wolpe, Noham; Zhang, Jiaxiang; Nombela, Cristina; Ingram, James N.; Wolpert, Daniel M.; Rowe, James B.; Tyler, Lorraine K.; Brayne, Carol; Bullmore, Edward T.; Calder, Andrew C.; Cusack, Rhodri; Dalgleish, Tim; Duncan, John; Matthews, Fiona E.; Marslen-Wilson, William D.; Shafto, Meredith A.; Cheung, Teresa; Geerligs, Linda; McCarrey, Anna; Mustafa, Abdur; Price, Darren; Samu, David; Treder, Matthias; Tsvetanov, Kamen A.; van Belle, Janna; Williams, Nitin; Bates, Lauren; Gadie, Andrew; Gerbase, Sofia; Georgieva, Stanimira; Hanley, Claire; Parkin, Beth; Troy, David; Auer, Tibor; Correia, Marta; Gao, Lu; Green, Emma; Henriques, Rafael; Allen, Jodie; Amery, Gillian; Amunts, Liana; Barcroft, Anne; Castle, Amanda; Dias, Cheryl; Dowrick, Jonathan; Fair, Melissa; Fisher, Hayley; Goulding, Anna; Grewal, Adarsh; Hale, Geoff; Hilton, Andrew; Johnson, Frances; Johnston, Patricia; Kavanagh-Williamson, Thea; Kwasniewska, Magdalena; McMinn, Alison; Norman, Kim; Penrose, Jessica; Roby, Fiona; Rowland...

Authors

Noham Wolpe

Jiaxiang Zhang

Cristina Nombela

James N. Ingram

Daniel M. Wolpert

James B. Rowe

Lorraine K. Tyler

Carol Brayne

Edward T. Bullmore

Andrew C. Calder

Rhodri Cusack

Tim Dalgleish

John Duncan

William D. Marslen-Wilson

Meredith A. Shafto

Teresa Cheung

Linda Geerligs

Anna McCarrey

Abdur Mustafa

Darren Price

David Samu

Matthias Treder

Kamen A. Tsvetanov

Janna van Belle

Nitin Williams

Lauren Bates

Andrew Gadie

Sofia Gerbase

Stanimira Georgieva

Claire Hanley

Beth Parkin

David Troy

Tibor Auer

Marta Correia

Lu Gao

Emma Green

Rafael Henriques

Jodie Allen

Gillian Amery

Liana Amunts

Anne Barcroft

Amanda Castle

Cheryl Dias

Jonathan Dowrick

Melissa Fair

Hayley Fisher

Anna Goulding

Adarsh Grewal

Geoff Hale

Andrew Hilton

Frances Johnson

Patricia Johnston

Thea Kavanagh-Williamson

Magdalena Kwasniewska

Alison McMinn

Kim Norman

Jessica Penrose

Fiona Roby

Diane Rowland

John Sargeant

Maggie Squire

Beth Stevens

Aldabra Stoddart

Cheryl Stone

Tracy Thompson

Ozlem Yazlik

Dan Barnes

Marie Dixon

Jaya Hillman

Joanne Mitchell

Laura Villis



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 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.

Citation

Wolpe, N., Zhang, J., Nombela, C., Ingram, J. N., Wolpert, D. M., Rowe, J. B., …Villis, L. (2018). Sensory attenuation in Parkinson’s disease is related to disease severity and dopamine dose. Scientific reports, 8(1), https://doi.org/10.1038/s41598-018-33678-3

Journal Article Type Article
Publication Date Dec 1, 2018
Deposit Date Dec 8, 2023
Journal Scientific Reports
Print ISSN 2045-2322
Electronic ISSN 2045-2322
Publisher Nature Publishing Group
Volume 8
Issue 1
DOI https://doi.org/10.1038/s41598-018-33678-3
Public URL https://hull-repository.worktribe.com/output/4452484