Beta synchrony in the cortico-basal ganglia network during regulation of force control on and off dopamine

Petra Fischer; Alek Pogosyan; Alexander L. Green; Tipu Z. Aziz; Jonathan Hyam; Thomas Foltynie; Patricia Limousin; Ludvic Zrinzo; Michael Samuel; Keyoumars Ashkan; Mauro Da Lio; Mariolino De Cecco; Alberto Fornaser; Peter Brown; Huiling Tan

Neurobiology of Disease (Jul 2019)

Beta synchrony in the cortico-basal ganglia network during regulation of force control on and off dopamine

Petra Fischer,
Alek Pogosyan,
Alexander L. Green,
Tipu Z. Aziz,
Jonathan Hyam,
Thomas Foltynie,
Patricia Limousin,
Ludvic Zrinzo,
Michael Samuel,
Keyoumars Ashkan,
Mauro Da Lio,
Mariolino De Cecco,
Alberto Fornaser,
Peter Brown,
Huiling Tan

Affiliations

Petra Fischer: Medical Research Council Brain Network Dynamics Unit, University of Oxford, OX1 3TH Oxford, UK; Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, OX3 9DU Oxford, UK; Corresponding author at: Nuffield Department of Clinical Neurosciences, Level 6, West Wing, John Radcliffe Hospital, Oxford OX3 9DU, UK.
Alek Pogosyan: Medical Research Council Brain Network Dynamics Unit, University of Oxford, OX1 3TH Oxford, UK; Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, OX3 9DU Oxford, UK
Alexander L. Green: Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, OX3 9DU Oxford, UK
Tipu Z. Aziz: Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, OX3 9DU Oxford, UK
Jonathan Hyam: Unit of Functional Neurosurgery, Department of Clinical and Movement Neurosciences, University College London Institute of Neurology, WC1N 3BG London, UK
Thomas Foltynie: Unit of Functional Neurosurgery, Department of Clinical and Movement Neurosciences, University College London Institute of Neurology, WC1N 3BG London, UK
Patricia Limousin: Unit of Functional Neurosurgery, Department of Clinical and Movement Neurosciences, University College London Institute of Neurology, WC1N 3BG London, UK
Ludvic Zrinzo: Unit of Functional Neurosurgery, Department of Clinical and Movement Neurosciences, University College London Institute of Neurology, WC1N 3BG London, UK
Michael Samuel: Departments of Neurology and Neurosurgery, King's College Hospital, King's College London, SE5 9RS London, UK
Keyoumars Ashkan: Departments of Neurology and Neurosurgery, King's College Hospital, King's College London, SE5 9RS London, UK
Mauro Da Lio: Department of Industrial Engineering, Università degli Studi di Trento, via Sommarive, 9, 38123 Trento, Italy
Mariolino De Cecco: Department of Industrial Engineering, Università degli Studi di Trento, via Sommarive, 9, 38123 Trento, Italy
Alberto Fornaser: Department of Industrial Engineering, Università degli Studi di Trento, via Sommarive, 9, 38123 Trento, Italy
Peter Brown: Medical Research Council Brain Network Dynamics Unit, University of Oxford, OX1 3TH Oxford, UK; Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, OX3 9DU Oxford, UK
Huiling Tan: Medical Research Council Brain Network Dynamics Unit, University of Oxford, OX1 3TH Oxford, UK; Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, OX3 9DU Oxford, UK

Journal volume & issue: Vol. 127
pp. 253 – 263

Abstract

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Beta power suppression in the basal ganglia is stronger during movements that require high force levels and high movement effort but it has been difficult to dissociate the two. We recorded scalp EEG and basal ganglia local field potentials in Parkinson's disease patients (11 STN, 7 GPi) ON and OFF dopaminergic medication while they performed a visually-guided force matching task using a pen on a force-sensitive graphics tablet. Force adjustments were accompanied by beta power suppression irrespective of whether the force was increased or reduced. Before the adjustment was completed, beta activity returned. High beta power was specifically associated with slowing of the force adjustment. ON medication, the peak force rate was faster and cortico-basal ganglia beta phase coupling was more readily modulated. In particular, phase decoupling was stronger during faster adjustments. The results suggest that beta power in the basal ganglia does not covary with force per se, but rather with a related factor, the absolute force rate, or a more general concept of movement effort. The results also highlight that beta activity reappears during stabilization of isometric contractions, and that dopamine-related suppression of cortico-basal ganglia beta coupling is linked to faster force adjustments.

Published in Neurobiology of Disease

ISSN: 0969-9961 (Print); 1095-953X (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry
Website: https://www.journals.elsevier.com/neurobiology-of-disease

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