Motor unit recruitment by size does not provide functional advantages for motor performance

Abstract

Key points• Motor unit recruitment according to size (orderly recruitment) is almost universally observed in human muscles.• Using genetic optimization methods on neuromuscular models, we explored the functional basis for orderly recruitment.• We show that the key features for optimal muscle performance are the number of motor neurons innervating the muscle and the distribution of their innervation numbers, and that a random recruitment order is as effective as a recruitment ordered by size.• This implies that size-ordered recruitment of motor neurons universally arises due to its intrinsic linkage to innervation number and not for function optimization.• These findings have implications for our understanding of human neural control of movement.Abstract It is commonly assumed that the orderly recruitment of motor units by size provides a functional advantage for the performance of movements compared with a random recruitment order. On the other hand, the excitability of a motor neuron depends on its size and this is intrinsically linked to its innervation number. A range of innervation numbers among motor neurons corresponds to a range of sizes and thus to a range of excitabilities ordered by size. Therefore, if the excitation drive is similar among motor neurons, the recruitment by size is inevitably due to the intrinsic properties of motor neurons and may not have arisen to meet functional demands. In this view, we tested the assumption that orderly recruitment is necessarily beneficial by determining if this type of recruitment produces optimal motor output. Using evolutionary algorithms and without any a priori assumptions, the parameters of neuromuscular models were optimized with respect to several criteria for motor performance. Interestingly, the optimized model parameters matched well known neuromuscular properties, but none of the optimization criteria determined a consistent recruitment order by size unless this was imposed by an association between motor neuron size and excitability. Further, when the association between size and excitability was imposed, the resultant model of recruitment did not improve the motor performance with respect to the absence of orderly recruitment. A consistent observation was that optimal solutions for a variety of criteria of motor performance always required a broad range of innervation numbers in the population of motor neurons, skewed towards the small values. These results indicate that orderly recruitment of motor units in itself does not provide substantial functional advantages for motor control. Rather, the reason for its near-universal presence in human movements is that motor functions are optimized by a broad range of innervation numbers.

Relative contribution of different altered motor unit control to muscle weakness in stroke: a simulation study

“…Unlike the condition of recruitment compression, additional forces are originated from increased firing rate at higher excitation levels, the overall force can still be reached to the required levels with random recruitment, because additionally recruited MUs are a mixture of small-fatigue-resistance to large-fatigable MUs, which can potentially maintain high force output. Consistent with an earlier simulation study [26], our findings indicate that the orderly recruitment based on MU size does not help improve the performance in force production.…”

Multiscale modeling of the neuromuscular system: Coupling neurophysiology and skeletal muscle mechanics

“…For example, based on the relation between the synaptic input to a motor neuron and its output discharge rate, Heckman and Binder (1991) and Fuglevand et al (1993) have proposed powerful phenomenological models for animal and human motor neurons, respectively. These models have been used extensively for the testing of neurophysiological hypotheses or for interpreting experimental data (Dideriksen et al, 2012;Dideriksen, Negro, Enoka, & Farina, 2011;Dideriksen & Farina, 2013;Dideriksen, Farina, Baekgaard, & Enoka, 2010;Jones, Hamilton, & Wolpert, 2002;Enoka et al, 2003;Yao, Fuglevand, & Enoka, 2000). However, one important limitation of phenomenological motor neuron models is the fact that they are not capable of naturally describing the membrane dynamics of the motor neurons, where nonlinear behavior of αMNs predominantly originates.…”

Higher muscle fiber conduction velocity and early rate of torque development in chronically strength-trained individuals

“…The primary determinant of motor unit twitch force is the number of muscle fibers innervated by the axon (13,52). Motor unit peak twitch forces in humans range from ~6 to ~78 mN•m with maximal tetanic forces ranging from ~30 to ~200 mN•m (32,34).…”