Reorganization of motor unit discharge-state space during ischemia-assisted fatigue: an energy landscape analysis

Abstract

Abstract

Neuromuscular fatigue increases variability in motor-unit (MU) discharge and force output, yet how it reorganizes population-level MU discharge dynamics remains poorly understood. Conventional analytical approaches primarily quantify discharge magnitude, variability, and common synaptic input, providing limited information regarding the organization of discharge-state space. Hence, we applied a time-resolved energy landscape framework that preserves a joint representation of the mean and variability of pooled MU discharge to characterize fatigue-related reorganization of population-level MU discharge-state space. This approach was motivated by the premise that force steadiness depends on the joint organization of neural drive level and neural drive variability. Force output and decomposed surface electromyographic signals were recorded during submaximal isometric wrist extension before and after an ischemia-assisted fatigue protocol in forty healthy adults. Thirty-five participants exhibiting post-fatigue reductions in maximal voluntary contraction force were included in subsequent analyses. Pooled MU discharge activity was represented by the instantaneous mean firing rate and analyzed using a sliding-window approach. Energy landscapes were constructed in a two-dimensional discharge-state space defined by the mean and variability of pooled MU discharge activity, enabling quantification of landscape structure (basin number, basin area, and basin depth) and state-space occupancy (centroid location and centroid dispersion). Fatigue significantly increased force fluctuation magnitude ( P < 0.001) and altered the organization of MU discharge-state space. Specifically, fatigue increased the number ( P = 0.017) and area ( P = 0.012) of attractor basins, indicating a broader distribution of preferred discharge configurations. Fatigue also induced significant shifts in centroid location ( P ≤ 0.008) and increased centroid dispersion ( P = 0.004), reflecting broader occupancy of discharge states. Furthermore, fatigue-related increases in force fluctuation magnitude were positively associated with basin area expansion ( r = 0.368, P = 0.030) and centroid dispersion ( r = 0.468, P = 0.005). Ischemia-assisted fatigue reorganized the state-space architecture of pooled MU discharge activity, resulting in broader discharge-state occupancy and reduced force steadiness. Energy landscape analysis provides a complementary time-resolved framework that preserves the joint evolution of the mean and variability of pooled MU discharge, offering a novel state-space perspective on fatigue-related decline in force stability.