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Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease

Activation of the basal ganglia has been shown during the preparation and execution of movement. However, the functional interaction of cortical and subcortical brain areas during movement and the relative contribution of dopaminergic striatal innervation remains unclear. We recorded local field pot...

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Autores principales: Canessa, Andrea, Pozzi, Nicolò G., Arnulfo, Gabriele, Brumberg, Joachim, Reich, Martin M., Pezzoli, Gianni, Ghilardi, Maria F., Matthies, Cordula, Steigerwald, Frank, Volkmann, Jens, Isaias, Ioannis U.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5138226/
https://www.ncbi.nlm.nih.gov/pubmed/27999534
http://dx.doi.org/10.3389/fnhum.2016.00611
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author Canessa, Andrea
Pozzi, Nicolò G.
Arnulfo, Gabriele
Brumberg, Joachim
Reich, Martin M.
Pezzoli, Gianni
Ghilardi, Maria F.
Matthies, Cordula
Steigerwald, Frank
Volkmann, Jens
Isaias, Ioannis U.
author_facet Canessa, Andrea
Pozzi, Nicolò G.
Arnulfo, Gabriele
Brumberg, Joachim
Reich, Martin M.
Pezzoli, Gianni
Ghilardi, Maria F.
Matthies, Cordula
Steigerwald, Frank
Volkmann, Jens
Isaias, Ioannis U.
author_sort Canessa, Andrea
collection PubMed
description Activation of the basal ganglia has been shown during the preparation and execution of movement. However, the functional interaction of cortical and subcortical brain areas during movement and the relative contribution of dopaminergic striatal innervation remains unclear. We recorded local field potential (LFP) activity from the subthalamic nucleus (STN) and high-density electroencephalography (EEG) signals in four patients with Parkinson’s disease (PD) off dopaminergic medication during a multi-joint motor task performed with their dominant and non-dominant hand. Recordings were performed by means of a fully-implantable deep brain stimulation (DBS) device at 4 months after surgery. Three patients also performed a single-photon computed tomography (SPECT) with [(123)I]N-ω-fluoropropyl-2β-carbomethoxy-3β-(4-iodophenyl)nortropane (FP-CIT) to assess striatal dopaminergic innervation. Unilateral movement execution led to event-related desynchronization (ERD) followed by a rebound after movement termination event-related synchronization (ERS) of oscillatory beta activity in the STN and primary sensorimotor cortex of both hemispheres. Dopamine deficiency directly influenced movement-related beta-modulation, with greater beta-suppression in the most dopamine-depleted hemisphere for both ipsi- and contralateral hand movements. Cortical-subcortical, but not interhemispheric subcortical coherencies were modulated by movement and influenced by striatal dopaminergic innervation, being stronger in the most dopamine-depleted hemisphere. The data are consistent with a role of dopamine in shielding subcortical structures from an excessive cortical entrapment and cross-hemispheric coupling, thus allowing fine-tuning of movement.
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spelling pubmed-51382262016-12-20 Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease Canessa, Andrea Pozzi, Nicolò G. Arnulfo, Gabriele Brumberg, Joachim Reich, Martin M. Pezzoli, Gianni Ghilardi, Maria F. Matthies, Cordula Steigerwald, Frank Volkmann, Jens Isaias, Ioannis U. Front Hum Neurosci Neuroscience Activation of the basal ganglia has been shown during the preparation and execution of movement. However, the functional interaction of cortical and subcortical brain areas during movement and the relative contribution of dopaminergic striatal innervation remains unclear. We recorded local field potential (LFP) activity from the subthalamic nucleus (STN) and high-density electroencephalography (EEG) signals in four patients with Parkinson’s disease (PD) off dopaminergic medication during a multi-joint motor task performed with their dominant and non-dominant hand. Recordings were performed by means of a fully-implantable deep brain stimulation (DBS) device at 4 months after surgery. Three patients also performed a single-photon computed tomography (SPECT) with [(123)I]N-ω-fluoropropyl-2β-carbomethoxy-3β-(4-iodophenyl)nortropane (FP-CIT) to assess striatal dopaminergic innervation. Unilateral movement execution led to event-related desynchronization (ERD) followed by a rebound after movement termination event-related synchronization (ERS) of oscillatory beta activity in the STN and primary sensorimotor cortex of both hemispheres. Dopamine deficiency directly influenced movement-related beta-modulation, with greater beta-suppression in the most dopamine-depleted hemisphere for both ipsi- and contralateral hand movements. Cortical-subcortical, but not interhemispheric subcortical coherencies were modulated by movement and influenced by striatal dopaminergic innervation, being stronger in the most dopamine-depleted hemisphere. The data are consistent with a role of dopamine in shielding subcortical structures from an excessive cortical entrapment and cross-hemispheric coupling, thus allowing fine-tuning of movement. Frontiers Media S.A. 2016-12-06 /pmc/articles/PMC5138226/ /pubmed/27999534 http://dx.doi.org/10.3389/fnhum.2016.00611 Text en Copyright © 2016 Canessa, Pozzi, Arnulfo, Brumberg, Reich, Pezzoli, Ghilardi, Matthies, Steigerwald, Volkmann and Isaias. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Canessa, Andrea
Pozzi, Nicolò G.
Arnulfo, Gabriele
Brumberg, Joachim
Reich, Martin M.
Pezzoli, Gianni
Ghilardi, Maria F.
Matthies, Cordula
Steigerwald, Frank
Volkmann, Jens
Isaias, Ioannis U.
Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease
title Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease
title_full Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease
title_fullStr Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease
title_full_unstemmed Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease
title_short Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease
title_sort striatal dopaminergic innervation regulates subthalamic beta-oscillations and cortical-subcortical coupling during movements: preliminary evidence in subjects with parkinson’s disease
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5138226/
https://www.ncbi.nlm.nih.gov/pubmed/27999534
http://dx.doi.org/10.3389/fnhum.2016.00611
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