Motor Unit Activity during Fatiguing Isometric Muscle Contraction in Hemispheric Stroke Survivors

Abstract

Enhanced muscle weakness is commonly experienced following stroke and may be accompanied by increased susceptibility to fatigue. To examine the contributions of central and peripheral factors to isometric muscle fatigue in stroke survivors, this study investigates changes in motor unit (MU) mean firing rate, and action potential duration during, and directly following, a sustained submaximal fatiguing contraction at 30% maximum voluntary contraction (MVC). A series of short contractions of the first dorsal interosseous muscle were performed pre- and post-fatigue at 20% MVC, and again following a 10-min recovery period, by 12 chronic stroke survivors. Individual MU firing times were extracted using surface EMG decomposition and used to obtain the spike-triggered average MU action potential waveforms. During the sustained fatiguing contraction, the mean rate of change in firing rate across all detected MUs was greater on the affected side (-0.02 ± 0.03 Hz/s) than on the less-affected side (-0.004 ± 0.003 Hz/s, p = 0.045). The change in firing rate immediately post-fatigue was also greater on the affected side than less-affected side (-13.5 ± 20 and 0.1 ± 19%, p = 0.04). Mean MU firing rates increased following the recovery period on the less-affected side when compared to the affected side (19.3 ± 17 and 0.5 ± 20%, respectively, p = 0.03). MU action potential duration increased post-fatigue on both sides (10.3 ± 1.2 to 11.2 ± 1.3 ms on the affected side and 9.9 ± 1.7 to 11.2 ± 1.9 ms on the less-affected side, p = 0.001 and p = 0.02, respectively), and changes in action potential duration tended to be smaller in subjects with greater impairment (p = 0.04). This study presents evidence of both central and peripheral fatigue at the MU level during isometric fatiguing contraction for the first time in stroke survivors. Together, these preliminary observations indicate that the response to an isometric fatiguing contraction differs between the affected and less-affected side post-stroke, and may suggest that central mechanisms observed here as changes in firing rate are the dominant processes leading to task failure on the affected side.

The Relationship Between Blood Flow and Motor Unit Firing Rates in Response to Fatiguing Exercise Post-stroke

“…Individuals with stroke, however, showed greater decreases in voluntary activation (Figure 3), less increase in EMG RMS, and less motor unit rate modulation (Figure 8) compared to the controls. These metrics indicate some combination of decreases from descending motor command and excitatory afferent inputs, as well as increases from inhibitory afferent inputs, to the motoneuron (Gandevia, 2001; Riley and Bilodeau, 2002; Knorr et al, 2011; Bowden et al, 2014; McManus et al, 2017). We also observed that greater increases in blood flow correlated with longer task duration only for the control group (Figure 6).…”

“…Electrophysiological studies using transcranial magnetic stimulation have shown this may be due to a loss of excitatory descending drive most likely caused by the stroke-related lesions to the motor cortex (Foltys et al, 2003; Jang et al, 2017; Peters et al, 2017). Based on studies showing decreased excitability in descending motor pathways, it is not surprising that recent evidence suggests that in people with stroke, central fatigue is a more significant contributor to fatigability of the paretic leg muscles than for the non-paretic legs and healthy controls (Riley and Bilodeau, 2002; Hu et al, 2006; Klein et al, 2010; Knorr et al, 2011; Hyngstrom et al, 2012; Bowden et al, 2014; Rybar et al, 2014; Kuhnen et al, 2015; McManus et al, 2017). These studies attribute force generating deficits to baseline reductions in cortical commands, but they do not consider the impact of the build-up of metabolic by-products on muscle function that could contribute to increased fatigability of limb muscles.…”

Analysis and Biophysics of Surface EMG for Physiotherapists and Kinesiologists: Toward a Common Language With Rehabilitation Engineers

“…Simultaneous sEMG and muscle force recordings during isometric muscle contractions may provide a more objective method of assessing local muscle fatigue in the clinic when compared with subjective mechanical techniques. Changes in the amplitude and the mean/median frequency of the sEMG signal can also provide insight into the relative prevalence of central 5 and peripheral fatigue 6 in neuromuscular disorders ( 40 ). An inability to sustain a voluntary, submaximal muscle contraction combined with a minimal decrease in the sEMG median frequency could indicate that the impairment is central in origin, arising from a suboptimal voluntary drive from brain to muscle.…”

Flexor Dysfunction Following Unilateral Transient Ischemic Brain Injury Is Associated with Impaired Locomotor Rhythmicity

“…It is likely that this imbalance of excitation and inhibition also causes changes in the potentiation and firing properties of the motor neurons themselves, ultimately leading to an impaired lower motor neuron recruitment which is remarkably biased towards the paretic side, inducing spasticity, high fatigability, and low motor unit recruitment rate 20,21 . A hyperactive clonus has sometimes been hypothesized to be induced by the seemingly chaotic reorganization of the supraspinal centers' patterning spinal structure, and haphazard pairing of the different interneuronal types driving type I and type II fibers with their presynaptic centers 22 .…”

“…Other means to assess motor function after neurological injury involve the investigation of muscular synergies using surface electromyographic recordings 20,[45][46][47] . These methods require technical skill which involves mathematical computation and decomposition of EMG data, which proves sufficient for the evaluation of synergistic impairments in post-stroke patients, but is of little use in the experimental setting, where the most common models are the rodent models.…”