The decoding of extensive samples of motor units in human muscles reveals the rate coding of entire motoneuron pools

Abstract

AbstractTo advance our understanding of the neural control of muscle, we decoded the firing activity of extensive samples of motor units in the Tibialis Anterior (129±44 per participant; n=8) and the Vastus Lateralis (130±63 per participant; n=8) during isometric contractions of up to 80% of maximal force. From this unique dataset, we characterised the rate coding of each motor unit as the relation between its instantaneous firing rate and the muscle force, with the assumption that the linear increase in isometric force reflects a proportional increase in the net synaptic excitatory inputs received by the motoneuron. This relation was characterised with a natural logarithm function that comprised two phases. The initial phase was marked by a steep acceleration of firing rate, which was greater for low-than medium- and high-threshold motor units. The second phase comprised a linear increase in firing rate, which was greater for high-than medium- and low-threshold motor units. Changes in firing rate were largely non-linear during the ramp-up and ramp-down phases of the task, but with significant prolonged firing activity only evident for medium-threshold motor units. Contrary to what is usually assumed, our results demonstrate that the firing rate of each motor unit can follow a large variety of trends with force across the pool. From a neural control perspective, these findings indicate how motor unit pools use gain control to transform inputs with limited bandwidths into an intended muscle force.Significance statementMovements are performed by motoneurons transforming synaptic input into an activation signal that controls muscle force. The control signal is not linearly related to the net synaptic input, but instead emerges from interactions between ionotropic and neuromodulatory inputs to motoneurons. Critically, these interactions vary across motoneuron pools and differ between muscles. We decoded the activity of hundreds of motor units from electromyographic signals recorded in vivo in humans to derive the most comprehensive framework to date of motor unit activity during isometric contractions that spanned the entire operating range of two human leg muscles. Our results address several key gaps in knowledge in this field and, importantly, characterise the activity of entire motor unit populations for each muscle.