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

Authors

Andrea Canessa, Julius-Maximilian-Universitat
Nicolo G. Pozzi, Julius-Maximilian-Universitat
Gabriele Arnulfo, Julius-Maximilian-Universitat
Joachim Brumberg, Julius-Maximlian-Universitat
Martin M. Reich, Julius-Maximilian-Universitat
Gianni Pezzoli, Centro Parkinson
Maria F. Ghilardi, CUNY City College
Cordula Matthies, Julius-Maximilian-Universitat
Frank Steigerwald, Julius-Maximilian-Universitat
Jens Volkman, Julius-Maximilian-Universitat
Ioannis U. Isais, Julius-Maximilian-Universitat

Document Type

Article

Publication Date

12-6-2016

Abstract

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 [123I]N-&-fluoropropyl-2b-carbomethoxy-3b-(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 ipsiand 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.

Comments

This article was originally published in frontiers in Human Neuroscience, available at doi: 10.3389/fnhum.2016.00611.

This is an open-access article distributed under the terms of the Creative Commons Attribution License(CCBY).