Intrinsic properties of spinal motoneurons degrade ankle torque control in humans

Abstract

Motoneurons are the final common pathway for all motor commands and possess intrinsic electrical properties that must be tuned to control muscle across the full range of motor behaviors. Neuromodulatory input from the brainstem is likely essential for adapting motoneuron properties to match this diversity of motor tasks. A primary mechanism of this adaptation, control of dendritic persistent inward currents (PICs) in motoneurons by brainstem monoaminergic systems, generates both amplification and prolongation of synaptic inputs. While essential, there is an inherent tension between this amplification and prolongation. Although amplification by PICs allows for quick recruitment and acceleration of motoneuron discharge during discrete motor tasks, PICs must be deactivated to de-recruit motoneurons upon movement cessation. In contrast, during stabilizing or postural tasks, PIC-induced prolongation of synaptic inputs is likely critical for sustained motoneuron discharge. Here, we designed two motor tasks that show PIC amplification and prolongation may conflict and generate errors that degrade the precision of motor output in humans. This included a paradigm comprised of a discrete motor task superimposed atop a stabilizing task and a paradigm with muscle length-induced changes to the balance of excitatory and inhibitory inputs available for controlling PICs. We show that prolongation from PICs introduces deficits in ankle torque control and that these deficits are further degraded at shorter muscle lengths when PIC prolongation is greatest. These results highlight the necessity for inhibitory control of PICs and showcase issues that are introduced when inhibitory control is perturbed or constrained. Our findings suggest that, like sensory systems, errors are inherent in motor systems. These errors are not due to problems in the perception of movement-related sensory input but are embedded in the final stage of motor output.