Elsevier

Clinical Neurophysiology

Volume 124, Issue 11, November 2013, Pages 2257-2263
Clinical Neurophysiology

Electrical stimulation site influences the spatial distribution of motor units recruited in tibialis anterior

https://doi.org/10.1016/j.clinph.2013.04.015Get rights and content

Highlights

  • M-wave recruitment curves were constructed from responses to electrical stimulation applied over the tibialis anterior muscle belly or common peroneal nerve.

  • Stimulation over the muscle belly recruited motor units progressively from superficial to deep as stimulation amplitude increased.

  • Stimulation over the nerve trunk recruited superficial and deep motor units equally, regardless of stimulation amplitude.

Abstract

Objective

To compare the spatial distribution of motor units recruited in tibialis anterior (TA) when electrical stimulation is applied over the TA muscle belly versus the common peroneal nerve trunk.

Methods

Electromyography (EMG) was recorded from the surface and from fine wires in superficial and deep regions of TA. Separate M-wave recruitment curves were constructed for muscle belly and nerve trunk stimulation.

Results

During muscle belly stimulation, significantly more current was required to generate M-waves that were 5% of the maximal M-wave (Mmax; M5%max), 50% Mmax (M50%max) and 95% Mmax (M95%max) at the deep versus the superficial recording site. In contrast, during nerve trunk stimulation, there were no differences in the current required to reach M5%max, M50%max or M95%max between deep and superficial recording sites. Surface EMG reflected activity in both superficial and deep muscle regions.

Conclusions

Stimulation over the muscle belly recruited motor units from superficial to deep with increasing stimulation amplitude. Stimulation over the nerve trunk recruited superficial and deep motor units equally, regardless of stimulation amplitude.

Significance

These results support the idea that where electrical stimulation is applied markedly affects how contractions are produced and have implications for the interpretation of surface EMG data.

Introduction

Neuromuscular electrical stimulation (NMES) is used to restore movement or reduce muscle atrophy after trauma to sensorimotor pathways in the central nervous system (CNS). A common target for such NMES therapies is tibialis anterior (TA), a muscle that dorsiflexes the ankle and is often affected following trauma to the CNS (Liberson et al., 1961, Merletti et al., 1978, Chae et al., 2008). To activate TA, NMES can be applied over the muscle belly (Merletti et al., 1978, Tsang et al., 1994) or over the common peroneal (CP) nerve trunk near the head of the fibula (Liberson et al., 1961, Merletti et al., 1978, Stein et al., 2010). Regardless of the stimulation site, contractions are generated predominantly by the activation of motor axons beneath the stimulating electrodes; although the activation of sensory axons can also contribute to contractions of soleus (Klakowicz et al., 2006, Lagerquist and Collins, 2010, Bergquist et al., 2011a), vastus medialis and vastus lateralis (Bergquist et al., 2012). The primary aim of this study was to investigate whether there are differences in the spatial distribution of motor units recruited by the activation of motor axons during stimulation over the TA muscle belly versus the CP nerve trunk. Our goal was not to distinguish between the territories of single motor units, but rather to compare the spatial distribution of populations of motor units recruited by electrical stimulation applied at these two sites. Our approach also provided insight into how electromyographic (EMG) signals recorded from the surface of the skin reflect activity in the deep and superficial regions of the TA muscle.

Several studies have investigated the spatial distribution of motor units recruited when NMES is applied over a muscle belly (Vanderthommen et al., 2000, Farina et al., 2004, Mesin et al., 2010). Regardless of the approach used or the muscle tested, these studies support the contention that superficial motor units are preferentially recruited during stimulation over the muscle belly (for review see Maffiuletti, 2010, Bergquist et al., 2011b). Adams et al. (1993), however, used functional magnetic resonance imaging and showed that in some participants motor units were recruited in deep regions of the quadriceps, even at relatively low stimulation amplitudes, when NMES was applied over the muscle belly. Thus, although there are discrepancies between studies about how recruited motor units are distributed within a muscle during stimulation over a muscle belly, the general consensus is that superficial motor units, those closest to the stimulating electrodes, are recruited preferentially. Currently there are no comparable data on the spatial distribution of motor units recruited when electrical stimulation is applied over a nerve trunk.

In the present study, we recorded EMG activity (M-waves and H-reflexes) from TA using surface EMG and fine wires inserted into superficial and deep regions of the muscle. H-reflexes were evoked infrequently and when present were small, consistent with previous literature for TA (Schieppati, 1987, Zehr, 2002, Klakowicz et al., 2006); thus, these data are not reported. Rather than deliver the stimulation repetitively, as is done when NMES is used for rehabilitation, we delivered single pulses of stimulation to generate M-wave recruitment curves. In this way, we were able to characterise the progression of motor unit recruitment from when the stimulation was below threshold for any response, to that which evoked a maximal M-wave (Mmax). We predicted that as stimulation amplitude increased during stimulation over the muscle belly, recruitment would progress from motor units closest to the stimulating electrodes (superficial) to those farthest away (deep). This prediction is supported by the majority of studies in the literature, although it has not been tested by recording EMG from different depths of the stimulated muscle. For stimulation over the CP nerve trunk, we predicted that recruited motor units would be distributed evenly throughout the muscle regardless of stimulation amplitude. Our rationale for this prediction comes from the finding that stimulation over a nerve trunk in vivo recruits motor units randomly in relation to axon diameter (Doherty and Brown, 1993, Major and Jones, 2005). Thus, regardless of the spatial organization of motor unit types in TA (Henriksson-Larsen et al., 1983), motor unit recruitment during stimulation over the CP nerve trunk should be randomly distributed throughout the TA muscle. Based on these two predictions, three hypotheses were tested. Hypothesis (1) When stimulation is applied over the TA muscle belly, significantly less current will be required to achieve an M-wave of 5% Mmax (M5%max), an M-wave of 50% Mmax (M50%max) and 95% Mmax (M95%max) for the superficial compared to the deep recording site. Hypothesis (2) When stimulation is applied over the CP nerve trunk, the current required to achieve M5%max, M50%max and M95%max will not differ between the superficial and deep recording sites. Hypothesis (3) Regardless of stimulation site, the area of either Mmax or the largest evocable M-wave within the range of stimulator output will not be different between the superficial and deep recording sites. Accordingly, we anticipated that although it would require more current to activate deep versus superficial regions of TA during stimulation over the muscle belly, we would be able to fully activate all regions of this relatively small muscle before reaching maximal stimulator output for both stimulation sites. The results of this study contribute to the body of knowledge about how electrical stimulation generates muscle contractions and provides further evidence that where the stimulation is applied markedly affects how contractions are produced (see also Bergquist et al., 2011a, Bergquist et al., 2012).

Section snippets

Participants

Nine human participants (4 males and 5 females; age range: 20–48, 27.4 ± 8.4 [mean ± SD]), with no known neurological or musculoskeletal impairment, volunteered for this study after providing informed written consent. This project was approved by the Health Research Ethics Board at the University of Alberta.

Position

Participants were seated in the chair of a Biodex dynamometer (System 3, Biodex Medical Systems, Shirley, New York). All procedures were performed on the right leg with the hip at approximately

Results

Recruitment curves constructed from data collected from a single participant for stimulation over the TA muscle belly and the CP nerve trunk are shown in Fig. 3A and B, respectively. The right side of this figure shows all of the single sweeps of EMG (overlaid) used to generate the recruitment curves for each recording site. In this participant, during stimulation over the muscle belly, the recruitment curve for the surface and superficial recording sites were similar, however both were

Discussion

The primary aim of this study was to investigate whether there are differences in the spatial distribution of motor units recruited by the activation of motor axons during stimulation over the TA muscle belly versus the CP nerve trunk. Consistent with previous literature (Vanderthommen et al., 2000, Farina et al., 2004, Mesin et al., 2010), we found that stimulation over the muscle belly recruited superficial motor units first, with deeper regions of the muscle recruited with increasing

Acknowledgments

The authors thank Mr. Alejandro Ley for his technical support. This work was supported by the University of Alberta Centre for Neuroscience (YO), the University of Alberta Human Performance Scholarship Fund (YO), an Alberta Paraplegic Foundation PhD Studentship (AJB), Canadian Institute of Health Research (KMC), Alberta Innovates Health Solution (KMC) and a Natural Sciences and Engineering Council of Canada Discovery Grant (DFC).

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