Force variability is mostly not motor noise: Theoretical implications for motor control.

Akira Nagamori,Christopher M Laine,Christopher M Laine,Gerald E Loeb,Francisco J Valero-Cuevas,Francisco J Valero-Cuevas

doi:10.1371/journal.pcbi.1008707

Abstract

Variability in muscle force is a hallmark of healthy and pathological human behavior. Predominant theories of sensorimotor control assume ‘motor noise’ leads to force variability and its ‘signal dependence’ (variability in muscle force whose amplitude increases with intensity of neural drive). Here, we demonstrate that the two proposed mechanisms for motor noise (i.e. the stochastic nature of motor unit discharge and unfused tetanic contraction) cannot account for the majority of force variability nor for its signal dependence. We do so by considering three previously underappreciated but physiologically important features of a population of motor units: 1) fusion of motor unit twitches, 2) coupling among motoneuron discharge rate, cross-bridge dynamics, and muscle mechanics, and 3) a series-elastic element to account for the aponeurosis and tendon. These results argue strongly against the idea that force variability and the resulting kinematic variability are generated primarily by ‘motor noise.’ Rather, they underscore the importance of variability arising from properties of control strategies embodied through distributed sensorimotor systems. As such, our study provides a critical path toward developing theories and models of sensorimotor control that provide a physiologically valid and clinically useful understanding of healthy and pathologic force variability.

Highlights

Variability is a hallmark of healthy and pathological human behavior
Our new computational model of a population of motor units demonstrates that nonphysiological assumptions in previous models have led to erroneous interpretations of the role and significance of motor unit properties in the generation of force variability
We developed a new model of a population of motor units that includes three physiologically important features: 1) calcium kinetics and cross-bridge dynamics that drives fusion of motor unit twitches, 2) coupling among motoneuron discharge rate, crossbridge dynamics, and muscle mechanics, and 3) a series-elastic element to account for the aponeurosis and tendon

Summary

Introduction

Variability is a hallmark of healthy and pathological human behavior. As such, the structure of kinematic [1] and kinetic variability [2, 3] is a rich behavioral phenomenon that informs theoretical models about the mechanisms used by the central nervous system to learn and produce motor behaviors [4,5,6,7,8,9,10,11,12,13,14]. Many theoretical models for human motor behavior (e.g. minimum variance theory and optimal control theory) assume that observed kinematic variability arises predominantly, if not exclusively, from ‘signal-dependent motor noise;’ random variations in muscle force output whose amplitude increases with the input level [5,6,7,8,9, 11,12,13,14, 17, 18] Under this theoretical framework, observed kinematics and its variability reflect the performance limitation imposed by the motor system [6, 18] attempting to minimize the deleterious effects of ‘motor noise’ on behavior [12, 17]. Many clinical manifestations of increased force/kinematic variability have been interpreted as a consequence of increased motor noise interfering with optimal control strategies implemented by the central nervous system [15, 19, 20]

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