Anα-MN collateral toγ-MNs can mitigate velocity-dependent stretch reflexes during voluntary movement: A computational study

Abstract

AbstractThe primary motor cortex does not uniquely or directly produceα-MN drive to muscles during voluntary movement. Rather,α-MN drive emerges from the synthesis and competition among excitatory and inhibitory inputs from multiple descending tracts, spinal interneurons, sensory inputs, and proprioceptive afferents. One such fundamental input is velocity-dependent stretch reflexes in lengthening (antagonist) muscles, which are thought to be inhibited by the shortening (agonist) muscles. It remains an open question, however, the extent to which velocity-dependent stretch reflexes disrupt voluntary movement, and whether and how they are inhibited in limbs with numerous mono- and multi-articular muscles where agonist and antagonist roles become unclear and can switch during a movement. We used a computational model of aRhesus Macaquearm to simulate movements with feedforwardα-MN commands only, and with added velocity-dependent stretch reflex feedback. We found that velocity-dependent stretch reflex caused movement-specific, typically large and variable disruptions to the arm endpoint trajectories. In contrast, these disruptions became small when the velocity-dependent stretch reflexes were simply scaled by theα-MN drive to each muscle (equivalent to anα-MN excitatory collateral to its homologousγ-MNs, but distinct fromα − γco-activation). We argue this circuitry is more neuroanatomically tenable, generalizable, and scalable thanα − γco-activation or movement-specific reciprocal inhibition. We propose that this mechanism at the homologous propriospinal level, by locally and automatically regulating the highly nonlinear neuro-musculo-skeletal mechanics of the limb, could be a critical low-level enabler of learning, adaptation, and performance via cerebellar and cortical mechanisms.SignificanceThe problem of muscle afferentation has long been an unsolved problem, and a foundation of voluntary motor control. How unmodulated velocity-dependent stretch reflexes disrupt voluntary movement and how they should be inhibited in limbs with numerous mono- and multi-articular muscles remain unclear. Here we demonstrate the cost of unregulated velocity-dependent reflexes, and propose a low-level propriospinal mechanism that can regularize these errors and enables motor learning and performance. Our results suggest that this spinal level mechanism of scaling dynamicγ-MN by the homologousα-MN collateral provides a generalizable mechanism that could be a low-level enabler of accurate and predictable movements that locally stabilizes and complements the synthesis and competition among cortical, subcortical or propriospinal projections toα-MN pools