Properties of oscillatory neuronal activity in the basal ganglia and thalamus in patients with Parkinson\u2019s disease

G Du,M Hallett,J.-Y Li,Y.-J Li,Y.-Q Zhang,P Zhuang

doi:10.1186/s40035-018-0123-y

Abstract

BackgroundThe cardinal features of Parkinson’s disease (PD) are bradykinesia, rigidity and rest tremor. Abnormal activity in the basal ganglia is predicted to underlie the mechanism of motor symptoms. This study aims to characterize properties of oscillatory activity in the basal ganglia and motor thalamus in patients with PD.MethodsTwenty-nine patients with PD who underwent bilateral or unilateral electrode implantation for subthalamic nucleus (STN) DBS (n = 11), unilateral pallidotomy (n = 9) and unilateral thalamotomy (n = 9) were studied. Microelectrode recordings in the STN, globus pallidus internus (GPi) and ventral oral posterior/ventral intermediate of thalamus (Vop/Vim) were performed. Electromyography of the contralateral limbs was recorded. Single unit characteristics including interspike intervals were analyzed. Spectral and coherence analyses were assessed. Mean spontaneous firing rate (MSFR) of neurons was calculated. Analysis of variance and X2 test were performed.ResultsOf 76 STN neurons, 39.5% were 4–6 Hz band oscillatory neurons and 28.9% were β frequency band (βFB) oscillatory neurons. The MSFR was 44.2 ± 7.6 Hz. Of 62 GPi neurons, 37.1% were 4–6 Hz band oscillatory neurons and 27.4% were βFB neurons. The MSFR was 80.9 ± 9.6 Hz. Of 44 Vop neurons, 65.9% were 4–6 Hz band oscillatory neurons and 9% were βFB neurons. The MSFR was 24.4 ± 4.2 Hz. Of 30 Vim oscillatory neurons, 70% were 4–6 Hz band oscillatory neurons and 13.3% were βFB neurons. The MSFR was 30.3 ± 3.6 Hz. Further analysis indicated that proportion of βFB oscillatory neurons in STN and GPi was higher than that of similar neurons in the Vop and Vim (P < 0.05). Conversely, the proportion of 4–6 Hz band oscillatory neurons and tremor related neurons in the Vim and Vop was higher than that of STN and GPi (P < 0.05). The highest MSFR was for GPi oscillatory neurons whereas the lowest MSFR was for Vop oscillatory neurons (P < 0.005).ConclusionThe alterations in neuronal activity in basal ganglia play a critical role in generation of parkinsonism. β oscillatory activity is more prominent in basal ganglia than in thalamus suggesting that the activity likely results from dopaminergic depletion. While both basal ganglia and thalamus have tremor activity, the thalamus appears to play a more important role in tremor production, and basal ganglia β oscillatory activity might be the trigger.

Highlights

The cardinal features of Parkinson’s disease (PD) are bradykinesia, rigidity and rest tremor
76 neurons were identified from 16 subthalamic nucleus (STN), 62 neurons were identified from 9 globus pallidus (GPi) and 74 neurons were identified from 9 ventral oral posterior of thalamus (Vop)/ventral intermediate of thalamus (Vim) (44 Vop neurons and 30 Vim neurons)
The length of the mean durations of neuronal recordings showed no significant difference among four nuclei: 38.4 ± 24.2 s for STN; 27.6 ± 22.8 s for GPi, and 36.4 ± 27.8 s for Vop/Vim (P > 0.05)

Summary

Introduction

The cardinal features of Parkinson’s disease (PD) are bradykinesia, rigidity and rest tremor. The increased neuronal firing rate in the GPi and STN has been found in animal model of PD [3,4,5,6,7,8,9] and are supported by microelectrode recording studies in PD patients undergoing surgery for symptoms [10, 11]. These studies indicate that neuronal activities in the basal ganglia neurons are increased compared to normal. While some studies show decreased neuronal firing [18, 19], some studies found no firing rate change [20] and others show increase in firing rates [22]

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