Elsevier

Clinical Neurophysiology

Volume 111, Issue 2, 1 February 2000, Pages 344-349
Clinical Neurophysiology

Changes in motor cortex excitability during ipsilateral hand muscle activation in humans

https://doi.org/10.1016/S1388-2457(99)00243-6Get rights and content

Abstract

Objectives: To test whether unilateral hand muscle activation involves changes in ipsilateral primary motor cortex (M1) excitability.

Methods: Single- and paired-pulse transcranial magnetic stimulation (TMS) of the right hemisphere was used to evoke motor evoked potentials (MEPs) from the resting left abductor pollicis brevis (APB) in 9 normal volunteers. We monitored changes in motor threshold (MT), MEP recruitment, intracortical inhibition (ICI) and intracortical facilitation (ICF) while the ipsilateral right APB was either at rest or voluntarily activated. Spinal motoneuron excitability was assessed using F-wave recording procedures.

Results: Voluntary muscle activation of the ipsilateral APB significantly facilitated the MEPs and F-waves recorded from the contralateral APB. Facilitation was observed with muscle activation >50% of the maximum voluntary force and with stimulus intensities >20% above the individual resting motor threshold. Intracortical inhibition significantly decreased in the ipsilateral M1, while there was no significant change in intracortical facilitation during this maneuver.

Conclusions: Unilateral hand muscle activation changes the excitability of homotopic hand muscle representations in both the ipsilateral M1 and the contralateral spinal cord. While the large proportion of MEP facilitation most likely occurred at a spinal level, involvement of the ipsilateral hemisphere may have contributed to the enlargement of magnetic responses.

Introduction

Transcranial magnetic stimulation (TMS) of the human brain is widely used to assess motor cortex excitability in humans non-invasively. A single magnetic stimulus applied over the cerebral hemisphere evokes responses in contralateral limb muscles and in muscles supplied by cranial nerves (Barker et al., 1985, Hess et al., 1987, Schriefer et al., 1988, Hallett, 1996). These responses can be facilitated by weak voluntary contraction of the target muscle, an effect that has been attributed to both spinal and cortical mechanisms (Hess et al., 1986, Thompson et al., 1991, Maertens de Noordhout et al., 1992, Mazzocchio et al., 1994, Ridding et al., 1995, Mills and Kimiskidis, 1996). Likewise, facilitation has been described during voluntary contraction of homologous muscles while the target muscle itself was at rest (Hess et al., 1986, Zwarts, 1992, Meyer et al., 1995). One postulated mechanism is that voluntary contraction increases spinal cord motorneuron excitability so that a descending volley evokes a motorneuronal discharge larger than had the homologous muscle been at rest (Hess et al., 1986, Zwarts, 1992). The main point of debate is whether voluntary activation of small hand muscles involves changes in the ipsilateral M1.

Hess et al. (1986) was the first to demonstrate that the motor evoked potential (MEP) of the resting abductor digiti minimi (ADM) can be increased by strong contraction of the homologous ADM muscle. This facilitation of responses to brain stimulation has been attributed to increased excitability of motor pathways projecting to the resting contralateral hand muscle, most likely at the level of the spinal cord rather than the cerebral hemisphere. Subsequent TMS studies often relied on indirect findings to describe changes in ipsilateral motor cortex excitability. For instance, Stedman et al. (1998) reported increase in MEP size after cortical stimulation but not after stimulation over the spinal cord, concluding that a large component of the facilitation occurred cortically. Using a different approach, Tinazzi and Zanette (1998) compared the effect of homologous muscle activation on MEPs evoked by transcranial electrical stimulation (TES) with the facilitatory effect seen after TMS. TES activates corticospinal axons mainly within the white matter where they are relatively unaffected by changes in cortical excitability, while TMS preferentially activates corticospinal neurons transsynaptically within the M1. Since both the H-reflex and MEPs in response to TES were unaffected by homologous muscle activation, the authors concluded that the facilitation seen after TMS was due to cortical mechanisms. In contrast to these studies, Chiappa et al., 1991, Samii et al., 1997 found no MEP facilitation during homologous muscle activation.

The present report is an attempt to resolve this controversy. In particular, we were interested in whether unilateral hand muscle activation involves changes in the ipsilateral M1. We used a paired-pulse TMS paradigm that allows recognition of changes in intracortical network excitability thought to be mainly independent of subcortical influences (Kujirai et al., 1993, Ziemann et al., 1996). Conventional techniques were used to study changes in motor threshold, MEP recruitment, and spinal motorneuron excitability during this maneuver.

Section snippets

Subjects

Nine healthy normal volunteers (self-designated right handers; 4 men, 5 women) with a mean age of 39 years (range, 31–55 years) gave their written informed consent to participate in the study, all of whom completed the experimental procedure. The subjects underwent full clinical examination before the start of the experiments and the study protocol was approved by the NINDS Institutional Review Board.

Recording of EMG activity

We studied the effects in the left hand muscles after stimulation of the right motor cortex,

Single-pulse experiments

Forceful activation of the i-APB significantly facilitated MEPs in the c-APB as compared with the resting condition (Fig. 1; P<0.001). This facilitation was statistically significant only if the muscle activation was >50% of MVC (Fig. 2), and if stimulus intensities >120% rMT were used (Fig. 1). Fig. 3 shows representative MEPs from the c-APB at rest and during maximal abduction of the i-APB (stimulus intensity, 150% rMT; MVC). Significant MEP facilitation was also observed in the c-ADM muscle (

Discussion

Unilateral hand muscle activation changes the excitability of homotopic hand muscle representations in both the ipsilateral M1 and the contralateral spinal cord. While the large proportion of MEP facilitation most likely occurred at the spinal level, the involvement of the ipsilateral M1 may have contributed to the enlargement of magnetic responses.

Acknowledgements

We wish to thank D.G. Schoenberg for skillful editing. W.M. was supported by the Max-Kade-Foundation.

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