Computational demonstration of spinal circuit that modulates γ-MN activity via α-MN collateral mitigates the inevitable disruptions from velocity-dependent stretch reflexes during voluntary movements

Abstract

The primary motor cortex does not uniquely or directly produce alpha motoneurone (-MN) drive to muscles during voluntary movement. Rather, -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 muscles, which should be inhibited to enable voluntary movement. It remains an open question, however, the extent to which unmodulated stretch reflexes disrupt voluntary movement, and whether and how they are inhibited in limbs with numerous multi-articular muscles. We used a computational model of a Rhesus Macaque arm to simulate movements with feedforward -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 arm movements. These disruptions were greatly reduced when modulating velocity-dependent stretch reflex feedback (i) as per the commonly proposed (but yet to be clarified) idealized alpha-gamma (-{gamma}) co-activation or (ii) an alternative -MN collateral projection to homonymous{gamma} -MNs. We conclude that such -MN collaterals are a physiologically tenable, but previously unrecognized, propriospinal circuit in the mammalian fusimotor system. These collaterals could still collaborate with -{gamma} co-activation, and the few skeletofusimotor fibers ({beta}-MNs) in mammals, to create a flexible fusimotor ecosystem to enable voluntary movement. By locally and automatically regulating the highly nonlinear neuro-musculo-skeletal mechanics of the limb, these collaterals could be a critical low-level enabler of learning, adaptation, and performance via higher-level brainstem, cerebellar and cortical mechanisms. SignificanceMuscles have velocity sensors controlled by{gamma} -MNs that produce stretch reflexes which could disrupt voluntary limb movements. Whether and how severely those unmodulated stretch reflexes disrupt voluntary movement remains unclear, especially in realistic multi-articular limbs. Our neuromechanical simulations demonstrate that unmodulated stretch reflexes greatly disrupt movements. Modulating the stretch reflex by implementing an idealized version of a long-posited (but yet unclear) -{gamma} co-activation greatly mitigates those perturbations. However, a collateral from the -MN to the{gamma} -MN (which has been reported among motoneurones but not interpreted in this way) achieves similar functionality. Our results suggest this modulation of the intensity of the stretch reflex by the -MN collateral provides an effective mechanism to locally stabilize the disruptions from stretch reflexes.