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 behaviours. Neuromodulatory input from the brainstem is probably 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, PICs must be deactivated to derecruit motoneurons upon movement cessation. In contrast, during stabilizing or postural tasks, PIC-induced prolongation of synaptic inputs is critical for sustained motoneuron discharge. Here, we designed two motor tasks that challenged the inhibitory control of PICs, generating unduly PIC prolongation that increases variability in human torque control. This included a paradigm combining a discrete motor task with a stabilizing task and another involving muscle length-induced changes to the balance of excitatory and inhibitory inputs available for controlling PICs. We show that prolongation from PICs introduces difficulties in ankle torque control and that these difficulties 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 introduced when inhibitory control is 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. This has many implications relevant to clinical conditions (e.g. chronic stroke) where pathological shifts in monoamines may further amplify these errors. KEY POINTS: All motor commands are processed via spinal motoneurons, whose intrinsic electrical properties are adapted by brainstem neuromodulatory input. The effects of these neuromodulatory inputs (i.e. persistent inward currents; PICs) must be tightly regulated by inhibitory inputs to allow for the large repertoire of human motor behaviours. We designed two motor tasks to restrict the ability of inhibitory synaptic inputs to control PICs and show that this generates substantial errors that reduce the precision of motor output in humans. Our findings suggest that errors are inherent in motor systems and embedded in the final stage of motor output. This has many implications relevant to clinical conditions (e.g. chronic stroke) and may, speculatively, shed light on contributing factors to muscle cramps.

Keywords: impairment; motoneurons; motor control; motor unit; persistent inward current; sombrero.