Elsevier

Clinical Neurophysiology

Volume 118, Issue 10, October 2007, Pages 2176-2179
Clinical Neurophysiology

Disturbed surround inhibition in preclinical parkinsonism

https://doi.org/10.1016/j.clinph.2007.06.058Get rights and content

Abstract

Objective

Surround inhibition in the motor system is an essential mechanism for selective execution of desired movements. To evaluate the functional operation of surround inhibition in Parkinson disease, we performed a transcranial magnetic stimulation (TMS) study in the asymptomatic hands of hemiparkinsonism patients.

Methods

TMS was set to be triggered by self-initiated flexion of the index finger at different intervals from 3 to 2000 ms. Average motor evoked potential (MEP) amplitudes obtained from self-triggered TMS were normalized to average MEPs of control TMS at rest. Normalized MEP amplitudes of the patients’ self-triggered TMS sessions at different intervals were compared to those of the controls.

Results

During index finger flexion, MEP amplitudes from the little finger muscle were unchanged in normal subjects. However, they were enhanced in Parkinson patients, despite the absence of any motor disturbance.

Conclusions

These results suggest that the functional operation of surround inhibition is impaired in Parkinson disease. This disturbance may precede motor disturbance in Parkinson disease.

Significance

Impaired surround inhibition can be useful to detect preclinical parkinsonism.

Introduction

Surround inhibition, suppression of excitability in an area surrounding an activated neural network, is a physiological mechanism that focuses neuronal activity and selects an appropriate neuronal response. It is believed to be an essential mechanism in the motor system, where it can aid the selective execution of desired movements (Mink, 1996). Functional existence of surround inhibition is demonstrated in the human motor system, using transcranial magnetic stimulation (TMS) (Sohn and Hallett, 2004b). Motor evoked potential (MEP) amplitude of the little finger muscle was significantly suppressed during voluntary flexion of the index finger, despite an increase in spinal excitability (Sohn and Hallett, 2004b). Modulation of intracortical inhibition could assist the selection of desired movements (with reduced inhibition) as well as the prevention of unwanted movements (with increased inhibition) (Stinear and Byblow, 2003, Zoghi et al., 2003). A disturbance in surround inhibition with impaired modulation of intracortical inhibition was demonstrated in dystonia (Sohn and Hallett, 2004a, Stinear and Byblow, 2004), where co-contraction of surrounding muscles acts as a key mechanism (Vitek, 2002).

The basal ganglia play a major role in the selective performance of desired movements, presumably via the surround inhibition mechanism (Mink, 1996). During voluntary movements, enhanced corticosubthalamopallidal activity inhibits thalamic excitatory output to the motor cortex, providing tonic suppression of the motor cortex. Simultaneously other pallidal neurons projecting to the thalamus act to generate desired movements by decreasing their discharge through focused striatal output via the direct pathway, thereby removing tonic inhibition to the thalamus and releasing the ‘brake’ from the desired cortical generators (Mink, 1996). Therefore, lesions in the basal ganglia circuit often cause disturbances in the control of voluntary movement (Lee and Marsden, 1994). Parkinson disease (PD), which is caused by selective nigrostriatal dysfunction, could provide a good model for investigating the influence of basal ganglia dysfunction on surround inhibition in the motor system. Using an experimental setting similar to previous studies (Sohn and Hallett, 2004a, Sohn and Hallett, 2004b), we evaluated the functional operation of surround inhibition in the asymptomatic hands of hemiparkinsonism patients.

Section snippets

Subjects

Eleven patients with unilateral PD (4 men and 7 women; mean age 57 ± 2.4; range 46–67 yrs) and 8 age-matched right-handed healthy controls (5 men and 3 women; mean age 52 ± 3.8; range 39–67 yrs) participated in this study after giving their written informed consent. This study was approved by the Local Ethics Committee. All patients had never taken antiparkinson medications prior to this study. The diagnosis of PD was made according to the British Brain Bank criteria, and the severity of PD was

Results

The patients’ clinical characteristics are shown in Table 1. The mean symptom duration was 16 ± 3.1 (range 3–36) months. Mean UPDRS motor scale was 11 ± 1.0 (range 6–15). The tested asymptomatic hand was dominant in 8 patients and non-dominant in 3 patients.

All subjects performed index finger flexion selectively and briefly. Accordingly, off-line analysis of EMG recordings demonstrated that ADM was usually quiet or with low-level EMG during voluntary flexion of the index finger in patients

Discussion

As expected, during index finger flexion, MEPs of ADM were significantly enhanced in the patients’ asymptomatic hand, suggesting disturbed surround inhibition. Rigidity could be a main limitation of TMS studies performed on PD patients, since increased muscle tone often produces an enhancement of MEPs. Thus we performed this study on the patients’ asymptomatic hands, where the muscle tone was normal. Comparable background EMG activity of ADM excludes this kind of influence on the present

Acknowledgements

This work was supported by a faculty research grant of Yonsei University College of Medicine for 2003, and the Brain Korea 21 Project for Medical Science, Yonsei University.

References (16)

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