Electrical stimulation of the common peroneal nerve and its effects on the relationship between corticomuscular coherence and motor control in healthy adults

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Abstract

Background

Sensory input via neuromuscular electrical stimulation (NMES) may contribute to synchronization between motor cortex and spinal motor neurons and motor performance improvement in healthy adults and stroke patients. However, the optimal NMES parameters used to enhance physiological activity and motor performance remain unclear. In this study, we focused on sensory feedback induced by a beta-band frequency NMES (β-NMES) based on corticomuscular coherence (CMC) and investigated the effects of β-NMES on CMC and steady-state of isometric ankle dorsiflexion in healthy volunteers. Twenty-four participants received β-NMES at the peak beta-band CMC or fixed NMES (f-NMES) at 100 Hz on different days. NMES was applied to the right part of the common peroneal nerve for 20 min. The stimulation intensity was 95% of the motor threshold with a pulse width of 1 ms. The beta-band CMC and the coefficient of variation of force (Force CV) were assessed during isometric ankle dorsiflexion for 2 min. In the complementary experiment, we applied β-NMES to 14 participants and assessed beta-band CMC and motor evoked potentials (MEPs) with transcranial magnetic stimulation.

Results

No significant changes in the means of beta-band CMC, Force CV, and MEPs were observed before and after NMES conditions. Changes in beta-band CMC were correlated to (a) changes in Force CV immediately, at 10 min, and at 20 min after β-NMES (all cases, p < 0.05) and (b) changes in MEPs immediately after β-NMES (p = 0.01). No correlations were found after f-NMES.

Conclusions

Our results suggest that the sensory input via NMES was inadequate to change the beta-band CMC, corticospinal excitability, and voluntary motor output. Whereas, the β-NMES affects the relationship between changes in beta-band CMC, Force CV, and MEPs. These findings may provide the information to develop NMES parameters for neurorehabilitation in patients with motor dysfunction.

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Most cited references 47

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Modulation of human corticomotor excitability by somatosensory input.

Alain Kaelin-Lang, Andreas R. Luft, Lumy Sawaki … (2002)

In humans, somatosensory stimulation results in increased corticomotoneuronal excitability to the stimulated body parts. The purpose of this study was to investigate the underlying mechanisms. We recorded motor evoked potentials (MEPs) to transcranial magnetic stimulation (TMS) from abductor pollicis brevis (APB), first dorsal interosseous (FDI), and abductor digiti minimi (ADM) muscles. MEP amplitudes, recruitment curves (RC), intracortical inhibition (ICI), intracortical facilitation (ICF), resting (rMT) and active motor thresholds (aMT) were recorded before and after a 2-h period of ulnar nerve electrical stimulation at the wrist. Somatosensory input was monitored by recording somatosensory evoked potentials. To differentiate excitability changes at cortical vs. subcortical sites, we recorded supramaximal peripheral M-responses and MEPs to brainstem electrical stimulation (BES). In order to investigate the involvement of GABAergic mechanisms, we studied the influence of lorazepam (LZ) (a GABA(A) receptor agonist) relative to that of dextromethorphan (DM) (an NMDA receptor antagonist) and placebo in a double-blind design. We found that somatosensory stimulation increased MEP amplitudes to TMS only in the ADM, confirming a previous report. This effect was blocked by LZ but not by either DM or placebo and lasted between 8 and 20 min in the absence of (i) changes in MEPs elicited by BES, (ii) amplitudes of early somatosensory-evoked potentials or (iii) M-responses. We conclude that somatosensory stimulation elicited a focal increase in corticomotoneuronal excitability that outlasts the stimulation period and probably occurs at cortical sites. The antagonistic effect of LZ supports the hypothesis of GABAergic involvement as an operating mechanism.

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Cortical control of human motoneuron firing during isometric contraction.

R Salmelin, M Kajola, S Salenius … (1997)

We recorded whole scalp magnetoencephalographic (MEG) signals simultaneously with the surface electromyogram from upper and lower limb muscles of six healthy right-handed adults during voluntary isometric contraction. The 15- to 33-Hz MEG signals, originating from the anterior bank of the central sulcus, i.e., the primary motor cortex, were coherent with motor unit firing in all subjects and for all muscles. The coherent cortical rhythms originated in the hand motor area for upper limb muscles (1st dorsal interosseus, extensor indicis proprius, and biceps brachii) and close to the foot area for lower limb muscles (flexor hallucis brevis). The sites of origin corresponding to different upper limb muscles did not differ significantly. The cortical signals preceded motor unit firing by 12-53 ms. The lags were shortest for the biceps brachii and increased systematically with increasing corticomuscular distance. We suggest that the motor cortex drives the spinal motoneuronal pool during sustained contractions, with the observed cortical rhythmic activity influencing the timing of efferent commands. The cortical rhythms could be related to motor binding, but the rhythmic output may also serve to optimize motor cortex output during isometric contractions.

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Author and article information

Contributors

Tomofumi Yamaguchi:

ORCID: http://orcid.org/0000-0003-2206-8586

t.yamaguchi.ja@juntendo.ac.jp

Journal

Journal ID (nlm-ta): BMC Neurosci

Journal ID (iso-abbrev): BMC Neurosci

Title: BMC Neuroscience

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2202

Publication date (Electronic): 13 October 2021

Publication date PMC-release: 13 October 2021

Publication date Collection: 2021

Volume: 22

Electronic Location Identifier: 61

Affiliations

[1 ]GRID grid.440893.2, ISNI 0000 0004 0375 924X, Department of Physical Therapy, , Yamagata Prefectural University of Health Sciences, ; 260 Kamiyanagi, Yamagata, 990-2212 Japan

[2 ]GRID grid.268394.2, ISNI 0000 0001 0674 7277, Department of Anatomy and Structural Science, , Yamagata University School of Medicine, ; 2-2-2 Iida-Nishi, Yamagata, 990-9585 Japan

[3 ]GRID grid.256115.4, ISNI 0000 0004 1761 798X, Faculty of Rehabilitation, School of Health Sciences, , Fujita Health University, ; 1-98 Dengakugakubo, Kutsukake-cho, Toyoake, Aichi 470-1192 Japan

[4 ]GRID grid.258269.2, ISNI 0000 0004 1762 2738, Department of Physical Therapy, Faculty of Health Science, , Juntendo University, ; 2-1-1 Hongo, Bunkyo-ku, Tokyo, 113-8421 Japan

Author information

Tomofumi Yamaguchi http://orcid.org/0000-0003-2206-8586

Article

Publisher ID: 665

DOI: 10.1186/s12868-021-00665-w

PMC ID: 8513252

PubMed ID: 34645385

SO-VID: e057bd1f-f929-49f2-874e-a9e9a70957ee

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 13 January 2021

Date accepted : 1 October 2021

Funding

Funded by: Grant-in-Aid for Young Scientists

Award ID: 18K17723

Award Recipient : Tomofumi Yamaguchi

Custom metadata

ScienceOpen disciplines: Neurosciences

Keywords: neuromuscular electrical stimulation,beta-band stimulation,sensory input,corticomuscular coherence,isometric contraction,corticospinal excitability

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ScienceOpen disciplines: Neurosciences

Keywords: neuromuscular electrical stimulation, beta-band stimulation, sensory input, corticomuscular coherence, isometric contraction, corticospinal excitability

Electrical stimulation of the common peroneal nerve and its effects on the relationship between corticomuscular coherence and motor control in healthy adults

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Communication Through Coherence

Most cited references 47

A framework for the analysis of mixed time series/point process data--theory and application to the study of physiological tremor, single motor unit discharges and electromyograms.

Modulation of human corticomotor excitability by somatosensory input.

Cortical control of human motoneuron firing during isometric contraction.

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