Hyperactivity of Basal Ganglia in Patients With Parkinson's Disease During Internally Guided Voluntary Movements.

Veronika Filyushkina,Vadim Ushakov,Igor Pronin,Alexey Tomskiy,Valentin Popov,Rita Medvednik,Artem Batalov,Alexey Sedov

doi:10.3389/fneur.2019.00847

Abstract

The contribution of different brain areas to internally guided (IG) and externally triggered (ET) movements has been a topic of debate. It has been hypothesized that IG movements are performed mainly through the basal ganglia-thalamocortical loop while ET movements are through the cerebello-thalamocortical pathway. We hypothesized that basal ganglia activity would be modified in patients with Parkinson's disease during IG movement as compared with normal subjects. We used functional MRI (fMRI) to investigate the differences between IG and ET motor tasks. Twenty healthy participants and 20 Parkinson's disease patients (OFF-state) were asked to perform hand movements in response to sound stimuli (ET) and in advance of the stimuli (IG). We showed that ET movements evoked activation of a few large clusters in the contralateral motor areas: the sensorimotor and premotor cortex, supplementary motor area (SMA), insula, putamen, motor thalamus and ipsilateral cerebellum. IG movements additionally evoked activation of a large number of small clusters distributed in different brain areas including the parietal and frontal lobes. Comparison between the activity of Parkinson's disease patients and healthy volunteers showed few important differences. We observed that along with the activity of the posterior areas, an activation of the anterior areas of putamen was observed during IG movements. We also found hyperactivity of the ventral thalamus for both movements. These results showed that IG movements in PD patients were made with the involvement of both sensorimotor and associative basal ganglia-thalamocortical loops.

Highlights

The internal-external control hypothesis proposed that the cerebellum, parietal lobe, and lateral premotor cortex (PMC) would dominate during externally-triggered (ET) movements, whereas the basal ganglia (BG) and supplementary motor area (SMA) would show a predominant involvement in internally-guided (IG) movements [1]
We showed distinctions between externally triggered (ET) and internally guided (IG) motor behavior concerned the localization and cluster size of activated brain areas in healthy group
ET movements only activate the executive circuits of the motor system, i.e., the sensorimotor cortex, basal ganglia, thalamus, and cerebellum

Summary

Introduction

The internal-external control hypothesis proposed that the cerebellum, parietal lobe, and lateral premotor cortex (PMC) would dominate during externally-triggered (ET) movements, whereas the basal ganglia (BG) and supplementary motor area (SMA) would show a predominant involvement in internally-guided (IG) movements [1]. Clinical and experimental data has suggested that bradykinesia or slowness of movement initiation in Parkinson’s disease may reflect an impaired connection between the supplementary motor area and putamen [6]. Yu et al showed that putamen-SMA functional connectivity is enhanced in patients with PD [8]. Later disturbance in functional connectivity in the motor loop was found during IG but not ET movements in PD patients [7]. Electrophysiological studies in PD showed that BGTM circuit is involved in the preparation of both IG and ET movements but CC loop involved in the preparation of IG movement only [10]

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