Electrical stimulation site influences the spatial distribution of motor units recruited in tibialis anterior
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).
References (44)
- et al.
Reproducibility of the CMAP scan
J Electromyogr Kinesiol
(2011) - et al.
A numerical model of passive and active behavior of skeletal muscles
Comput Methods Appl Mech Eng
(1998) - et al.
Investigation of motor unit recruitment during stimulated contractions of tibialis anterior muscle
J Electromyogr Kinesiol
(2010) The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man
Prog Neurobiol
(1987)- et al.
Differences in cardiorespiratory and neuromuscular responses between voluntary and stimulated contractions of the quadriceps femoris muscle
Respir Physiol Neurobiol
(2007) - et al.
Chronic muscle stimulation improves ischaemic muscle performance in patients with peripheral vascular disease
Eur J Vasc Surg
(1994) - et al.
Mapping of electrical muscle stimulation using MRI
J Appl Physiol
(1993) - et al.
Recruitment order of motoneurons in stretch reflexes is highly correlated with their axonal conduction velocity
J Neurophysiol
(1984) - et al.
Motor unit rotation in a variety of human muscles
J Neurophysiol
(2009) - et al.
Rotation of motoneurons during prolonged isometric contractions in humans
J Neurophysiol
(2006)
Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: triceps surae
J Appl Physiol
Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley
Eur J Appl Physiol
Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: quadriceps femoris
J Appl Physiol
Atlas of the muscle motor points for the lower limb: implications for electrical stimulation procedures and electrode positioning
Eur J Appl Physiol
Anatomy and innervation ratios in motor units of cat gastrocnemius
J Physiol
The transient subthreshold response of spherical and cylindrical cell models to extracellular stimulation
IEEE Trans Biomed Eng
Neuromuscular electrical stimulation for motor restoration in hemiplegia
Top Stroke Rehabil
Effects of two types of fatigue on the VO(2) slow component
Int J Sports Med
The estimated numbers and relative sizes of thenar motor units as selected by multiple point stimulation in young and older adults
Muscle Nerve
M-Wave properties during progressive motor unit activation by transcutaneous stimulation
J Appl Physiol
Spinal and supraspinal factors in human muscle fatigue
Physiol Rev
Transcutaneous neuromuscular electrical stimulation: influence of electrode positioning and stimulus amplitude settings on muscular response
Eur J Appl Physiol
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