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-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.
Highlights
The functional interaction of cortical and subcortical brain areas during movement planning and execution, and in particular the role of striatal dopaminergic innervation, remains unclear
Based on molecular imaging and clinical data, we identified the hemisphere with less (STN− and motor cortex, motor cortices (MC)−) or more (STN+ and MC+) dopaminergic innervation
Our findings suggest that movement-related beta-modulation is dependent on striatal dopaminergic innervation
Summary
The functional interaction of cortical and subcortical brain areas during movement planning and execution, and in particular the role of striatal dopaminergic innervation, remains unclear. STN recordings reveal that when at rest, unmedicated PD patients show an excessively synchronized neuronal activity in the STN and an exaggerated coupling between the STN and the motor cortices (MC) This abnormal activity and coupling is strong in the beta frequency range (≈13–35 Hz) and is reduced by dopaminergic drugs or STN-DBS (Williams et al, 2002; Fogelson et al, 2006; Doyle Gaynor et al, 2008; Kühn et al, 2008; de Solages et al, 2010; Giannicola et al, 2010; Litvak et al, 2011a, 2012; Hirschmann et al, 2013; Kato et al, 2015; Quinn et al, 2015; Weiss et al, 2015; Oswal et al, 2016) and modulated by voluntary movements (Marsden et al, 2001; Cassidy et al, 2002; Lalo et al, 2008; Hirschmann et al, 2013). Excessive cortical beta power at rest has been recently correlated with greater movement-related beta-modulation and motor performances (Heinrichs-Graham and Wilson, 2016)
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