Role of spinal sensorimotor circuits in triphasic command: a simulation approach using Goal Exploration Process

Abstract

During rapid voluntary limb movement about a single joint, a stereotyped triphasic pattern is typically observed in the electromyograms (EMGs) of antagonistic muscles acting at this joint. To explain the origin of such triphasic commands, two types of theories have been proposed. Peripheral theories consider that triphasic commands result from sensorimotor spinal networks, either through a combination of reflexes or through a spinal central pattern generator. Central theories consider that the triphasic command is elaborated in the brain. Although both theories were partially supported by physiological data, there is still no consensus about how exactly triphasic commands are elaborated. Moreover, capacities of simple spinal sensorimotor circuits to elaborate triphasic commands on their own have not been tested yet. In order to test this, we modelled arm musculoskeletal system, muscle activation dynamics, proprioceptive spindle and Golgi afferent activities and spinal sensorimotor circuits. Step commands were designed to modify the activity of spinal neurons and the strength of their synapses, either to prepare (SET) the network before movement onset, or to launch the movement (GO). Since these step commands do not contain any dynamics, changes in muscle activities responsible for arm movement rest entirely upon interactions between the spinal network and the musculo-skeletal system. Critically, we selected step commands using a Goal Exploration Process inspired from baby babbling during development. In this task, the Goal Exploration Process proved very efficient at discovering step commands that enabled spinal circuits to handle a broad spectrum of functional behaviors, displayed in a behavioral space characterized by movement amplitude and maximal speed. All over the behavioral space, specific SET and GO commands elicited natural triphasic commands, thereby substantiating the inherent capacity of the spinal network in generating them. Key points SummaryO_LISpinal sensorimotor circuits, despite extensive physiological analyses, remain poorly understood in the context of voluntary movement. C_LIO_LIThis study models the capabilities of these spinal networks, alongside musculoskeletal dynamics, to achieve single-joint arm flexion following minimum jerk principles. C_LIO_LIPreparatory (SET) and launch (GO) step commands modulate spinal network states, including neuron activity and synaptic strength. C_LIO_LINotably, arm movement results from sensorimotor interactions within spinal circuits, even with basic step commands that have no dynamics. C_LIO_LIA Goal Exploration Process (GEP), inspired by developmental baby babbling through trial and error, was used to refine step commands. C_LIO_LIThe spinal networks, when in appropriate states, were shown to spontaneously generate triphasic commands across a broad range of valid movement amplitudes and speeds. C_LIO_LIThese findings highlight the intrinsic capacity of spinal sensorimotor circuits to manage complex movement dynamics, offering novel testable insights as to their possible functional role in voluntary motor control. C_LI