Introduction
Transcutaneous neuromuscular electrical stimulation (TNMES) is a method to electrically activate muscle fibers by applying stimulation electrodes on the skin above muscles and stimulating branches of motor nerve. TNMES is used to promote physiological and functional improvement in paralyzed limbs (Ragnarsson
2008; Sheffler and Chae
2007; Peckham and Knutson
2005) and counteract musculoskeletal atrophy (Bergquist et al.
2011; Dudley-Javoroski and Shields
2008). Without normal use, paralyzed muscle rapidly atrophies, creating a catabolic state, poor cosmesis, and increased risk for secondary complications (Shields and Cook
1992; Dudley-Javoroski and Shields
2008; Garber and Krouskop
1982; Chantraine et al.
1986; Merli et al.
1993), which ultimately can be life threatening (Shields and Dudley-Javoroski
2003,
2006). While TNMES has succeeded in assisting individuals with neuromuscular disorders, a critical limitation with this rehabilitative approach is the rapid onset of muscle fatigue during repeated contractions (Bickel et al.
2011; Shields and Dudley-Javoroski
2006; Mizrahi et al.
1997), which results in muscle force decay and slowing of muscle contractile properties (Jones
2010; Enoka and Stuart
1992).
The increased fatigability with TNMES is thought by some researchers to reflect a reversal of the size principle of recruitment (Henneman et al.
1965a,
b), when larger axons that innervate the more easily fatigable fibers are recruited at low stimulus magnitudes and the smaller axons follow with increased stimulation levels (Peckham and Knutson
2005; Sheffler and Chae
2007; Bickel et al.
2011). Another plausible explanation is that voluntary contraction allows work being shared between different motor units of the same muscle (Bajd et al.
1999; Bickel et al.
2011), whereas conventional TNMES does not permit alterations in recruitment of motor units because all parameters remain fixed during the bout (Bickel et al.
2011). Thus, in stimulated muscles, a synchronized and massive fiber contraction replaces the normal physiological mechanism of motor unit recruitment and firing rate regulation (De Luca
1984). Furthermore, in individuals with neuromuscular disorders, fatigue develops within the motor unit and is associated with such factors as depletion of substances, accumulation of catabolites, and problems in excitation–contraction coupling (Biering-Sorensen et al.
2009; Pelletier and Hicks
2009; Shields
1995). Due to these major factors, the paralyzed muscles show greater fatigability than healthy muscles (Gerrits et al.
1999,
2003; Lenman et al.
1989; Thomas
1997a,
b; Shields
1995), thus further compounding the problem of muscle fatigue during TNMES. Consequently, developing means to counter force loss during electrical stimulation has received much interest (Gauthier et al.
1992; Stein et al.
1992; Binder-Macleod and McLaughlin
1997; Riess and Abbas
2001).
Because synchronous activation of an entire muscle is one of the fundamental causes of rapid muscle fatigue during TNMES, it is logical to consider an approach where activating several subcomponents separately is used to reduce muscle fatigue. To achieve this indirectly, early attempts have included stimulation with stochastically modulated parameters such as pulse frequency and amplitude (Graham et al.
2006; Thrasher et al.
2005; Graupe et al.
2000). The results from these studies are not consistent: one study showed that stochastic modulation decreases fatigue (Graupe et al.
2000) and the other two studies showed no significant difference (Graham et al.
2006; Thrasher et al.
2005). In addition, reduced fatigue has been demonstrated using more direct approaches of separately activating subcompartments of muscles in nerve stimulation. This was achieved using multiple electrodes with each activating a different set of nerve fibers and stimulation pulses of relatively low frequencies were sent to each electrode, one after another, resulting in a fused response. This type of spatially distributed and sequentially applied stimulation is referred to as ‘sequential stimulation’ (Nguyen et al.
2011). Fatigue was reduced with such stimulation in animal experimental models using spinal stimulation (Petrofsky
1978,
1979; Mushahwar and Horch
1997), intrafascicular stimulation (McDonnall et al.
2004; Yoshida and Horch
1993), interfascicular stimulation (Thomsen and Veltink
1997), epineural stimulation (Petrofsky
1979), and intramuscular stimulation (Lau et al.
1995; Zonnevijlle et al.
2000; Lau et al.
2007).
To date, observations on this stimulation method in human subjects are limited to only a few studies (Malesevic et al.
2010; Pournezam et al.
1988) including a case report from our group (Nguyen et al.
2011). Pournezam et al. (
1988) applied sequential stimulation to three knee extensor muscles in two individuals using three active surface electrodes distributed over these muscles. Malesevic et al. (
2010) investigated fatigue reduction using sequential stimulation of the knee extensor muscles through four active surface electrodes distributed over quadriceps as compared to one active electrode. In these two studies (Malesevic et al.
2010; Pournezam et al.
1988), electrodes were spaced far apart, each of which intentionally targeted one motor point of three separate knee extensor synergists rather than allowing different, potentially overlapping, sets of motor units to be activated. Our recent pilot study with one individual with spinal cord injury (Nguyen et al.
2011) was unique in the sense that multiple active surface electrodes providing the interleaved stimulation were collocated at the same site and over the same area as during stimulation with one active electrode targeting a single motor point of a relatively small muscle, as opposed to the previously reported widely distributed electrode setup over the large muscles. We termed such stimulation over multiple active electrodes as spatially distributed sequential stimulation (SDSS). Through four active electrodes, SDSS was delivered by sending a stimulation pulse to each electrode one after another with 90° phase shift between successive electrodes. Single electrode stimulation (SES) was delivered through one active electrode for comparison. We demonstrated that the fatigue resistance improved almost twice in SDSS compared to SES. We hypothesize the effectiveness of the SDSS might be explained by different sets of muscle fibers being activated by different electrodes, and, therefore, the increased time between subsequent activation of motor units allows their greater recovery. However, verification of the obtained result with a larger number of subjects is required and the mechanism of this fatigue reduction is yet to be explored.
The first purpose of this study was to investigate the fatigue-reducing ability of SDSS in more detail, in particular, focusing on the muscle contractile properties and on a larger group of subjects (Experiment 1). The second purpose of this study was to investigate the mechanism of the fatigue-reducing effects of SDSS using array-arranged electromyogram (EMG), by measuring EMG in medial, median, and lateral portions of the soleus muscle in response to single stimuli delivered using SDSS and SES (Experiment 2).
Conclusion
The present work demonstrated that torque decay was negligible during the fatiguing stimulation using spatially distributed sequential stimulation in plantar flexor muscles for able-bodied individuals, whereas there was a marked torque decay during single active electrode stimulation. In addition, we demonstrated that the spatially distributed sequential stimulation did not affect much the muscle contractile properties during the fatiguing stimulation, whereas single active electrode stimulation slowed down muscle contraction progression and relaxation. These results suggest that muscle fatigue was negligible during spatially distributed sequential stimulation, but marked during single active electrode stimulation. Further, we demonstrated that during the spatially distributed sequential stimulation, the amplitude of the M-waves at each muscle portion is dependent on the location of the stimulation electrodes, suggesting that different sets of muscle fibers are activated alternatively by different electrodes, which is closer to physiological activation. We conclude that because of this, spatially distributed sequential stimulation is more effective in reducing muscle fatigue compared to single active electrode stimulation, which must have a prominent advantage in neurorehabilitation using transcutaneous neuromuscular electrical stimulation.