Firing properties of motor units during fatigue in subjects after stroke

Abstract

The purpose of this work was to investigate the electromyographic (EMG) fatigue representations in muscles of subjects after stroke at the level of motor unit, based on the analysis of mean power frequency (MPF) in the power density spectrum (PDS) for intramuscular EMG and our previous modeling and experiment studies on the neuromuscular transmission failure (NTF). NTF due to the local muscular fatigue had been captured in motor unit signals from healthy subjects during a submaximal fatigue contraction previously. In this study, the EMG signals for the biceps brachii muscles were collected by needle electrodes from the affected and unaffected arms of six hemiplegic subjects after stroke, and from the dominated arm of six healthy subjects during a full maximum voluntary contraction (MVC) and a subsequent 20% MVC. The MPF of EMG trials detected intramuscularly during the full and 20% MVCs, and the parameters of motor unit action potential trains (MUAPTs) during 20% MVC were analyzed in three groups: the normal (from healthy subjects), unaffected (from subjects after stroke), and affected (from subjects after stroke). It was found that during the full MVC the MPFs of the normal and unaffected groups decreased more than the affected when monitored by a moving time window of 2 s. The comparison on the overall MPF during the full MVC for these three groups over the whole time course of the EMG signal (18 s) were: the affected overall MPF was higher than the unaffected (P < 0.05); and the unaffected overall MPF was larger than the normal (P < 0.05). However, no significant decrease in MPF was found for these three groups during 20% MVC. The NTF was captured in most MUAPTs in the groups of the normal and unaffected rather than in the affected group, symbolized by the lowered rates of change (RCs) of firing rate (FR) (P < 0.05), more MUAPTs with positive RCs of maximum oscillation (MO) in MUAPT power density spectra (P < 0.05), and the significant higher RCs of minimum inter-pulse interval (MINI) (P < 0.05) in the normal and unaffected compared to the affected group. Enhanced neural drives to the motor units of the unaffected and affected groups were observed during 20% MVC, which possibly came from the bilateral neural inputs due to the disinhibition of the ipsilateral projections in subjects after stroke. For identifying the fatigue associated with NTF, the motor unit firing parameters, FR, MINI, and MO, were more sensitive than the MPF. The results obtained in this work provided a further understanding on the EMG of the fatigue processes in paretic and non-paretic muscles during voluntary contractions.

Introduction

Muscular fatigue has been defined bio-mechanically as an inability to maintain the expected force or power output [1]. The overall performance of a muscle under the control of the nervous system would be affected by the central and peripheral factors, such as the lowered subjective intention, the failure of the conduction of nerve impulses to muscle fibers, the inactivation of sarcolemma, etc., [2]. Electromyography (EMG) is a helpful tool for accessing the fatigue dynamics of individual muscles in vivo. According to Basmajian and DeLuca’s study, muscle fatigue was characterized by a shift in electromyographic spectral density towards lower frequencies while average EMG amplitude increased or was unaltered [3]. These characteristics of EMG signals during muscle fatigue have been widely used as a fatigue index in applications of sports medicine, neuromuscular rehabilitation, and even the control of neuroprosthetic devices [4], [5], [6].

However, most current knowledge on EMG properties during fatigue was based on the analysis on normal muscles. Only a few studies have documented myoelectric characteristics of fatigue in persons with hemiparesis due to stroke [7], [8], [9]. It is important to understand the differences of EMG properties during fatigue processes between the paretic muscles in subjects after stroke and non-paretic muscles, which is the prerequisite for the diverse applications of EMG technique in stroke rehabilitation. Different EMG characteristics have been reported in paretic muscles after stroke under certain fatigue protocols when compared to that of the normal or unaffected ones. Svantesson et al. [7] found that different from the observation in the unaffected muscles in subjects after stroke, a reduction in high-intensity dynamic muscle activity was not associated with a decrease in mean power frequency (MPF) in the affected muscles, when performing repetitive eccentric-concentric plantar flexions [7]. Non-significant decrease, or even no decrease, in median frequency of EMG during fatigue efforts of paretic muscles in subjects after stroke also has been documented, when comparable decreases in output forces were captured in both paretic and non-paretic control muscles during maximal voluntary contractions [9]. Toffola et al. [8] found the extent of the reduction of the median frequency of EMG in paretic muscles was less than that of the non-paretic muscles, when supramaximal tetanic electric stimulation was used to evoke myoelectricities [8]. Possible reasons proposed for such discrepancies in EMG activities between the paretic and non-paretic muscles after stroke could be the preferential atrophy of type II fibers, the decrease in the ability to activate muscles, and lowered motor unit synchronization following a stroke [10], [11], [12], [13]. In comparison with unimpaired neuromuscular systems, spasticity, weakness, and altered neural drives with varied extents were commonly observed in subjects after stroke, which would cause the consecutive neuromuscular changes, such as muscle stiffness, motor unit reduction, motor unit reinnervation, reduced firing rate, etc., [10], [11], [12], [13]. These variations would inevitably affect the EMG signals detected from subjects after stroke. As suggested by Svantesson et al. [7], there might be peripheral fatigue factors not reflected in the electromyographic activities if measured by MPF [7].

For interpretation of EMG signals, it is helpful to develop consistent theories that relate the elemental mechanisms affecting the generation of EMG to the observed signal changes. It has been well established that the decrease of MPFs during fatigue was mainly due to a reduction in the muscle fiber conduction velocity, and increased motor unit synchronization and recruitment [3], [14]; while the changes in motor unit mean firing rates, recruitment, and synchronization would affect the detected EMG amplitudes [15]. The variations in firing statistics of a single motor unit, e.g. mean firing rate or standard deviation of inter-pulse interval (IPI), were not directly related to the change of MPFs of the EMG spectra of the motor unit, giving a constant shape of the motor unit action potential (MUAP) [16]. Neuromuscular transmission failure (NTF), known as the stimulation arising from the motor neuron cannot successfully reach the muscle fibers under its innervation to evoke a detectable MUAP, was an important neuromuscular local property that affected the motor unit firing characteristics during muscle fatigue [17], [18]. NTF would occur at several pre- and post-synaptic sites, such as axonal branching points, pre-synaptic membrane of a neuromuscular junction, and sarcolemma due to the reduction of the excitability along the neuromuscular pathway and depletion of neurotransmitters [18]. NTF could be identified at the level of a whole motor unit, which was mainly caused by an increased motor unit refractory period during the fatigue [19], [20]. In our previous works, the effects of the varied motor unit refractoriness on the motor unit firing statistics and signal spectra have been analyzed by mathematical modeling, numerical simulation and a needle EMG experiment on normal biceps brachii muscles in healthy subjects by a fatigue protocol [19], [20]. NTF was captured in normal motor units during 20% maximal voluntary contractions (MVCs) of elbow flexion with a proceeded fatigue effort. It was also found that the increased refractoriness of a motor unit would result in a further extent of NTF, which would consequently cause a decrease in the firing rate, an increase or unchanged standard deviation of inter-pulse interval, and an enhanced oscillation in the power density spectra (PDS) of motor unit action potential trains (MUAPTs). However, the extent of the NTF in paretic muscles in subjects after stroke has not been investigated in comparison with that of the non-paretic ones. The NTF, decreased muscle fiber conduction velocity, and increases in motor unit synchronization and recruitment were physiological phenomena observed during muscle fatigue in healthy subjects. The NTF would cause variation in motor unit firing statistics, and the rest factors were found to mainly affect the MPF of the myoelectric signals. Based on our previous work of NTF on healthy subjects [19], [20], the purpose of this work was to investigate the fatigue representations in EMG of the paretic, and non-paretic muscles from both stroke and healthy subjects in the aspects of MPF and the myoelectric parameters related to the NTF during voluntary contractions.