The processing of proprioceptive signals in distributed networks: insights from insect motor control

Abstract

ABSTRACT The integration of sensory information is required to maintain body posture and to generate robust yet flexible locomotion through unpredictable environments. To anticipate required adaptations in limb posture and enable compensation of sudden perturbations, an animal's nervous system assembles external (exteroception) and internal (proprioception) cues. Coherent neuronal representations of the proprioceptive context of the body and the appendages arise from the concerted action of multiple sense organs monitoring body kinetics and kinematics. This multimodal proprioceptive information, together with exteroceptive signals and brain-derived descending motor commands, converges onto premotor networks – i.e. the local neuronal circuitry controlling motor output and movements – within the ventral nerve cord (VNC), the insect equivalent of the vertebrate spinal cord. This Review summarizes existing knowledge and recent advances in understanding how local premotor networks in the VNC use convergent information to generate contextually appropriate activity, focusing on the example of posture control. We compare the role and advantages of distributed sensory processing over dedicated neuronal pathways, and the challenges of multimodal integration in distributed networks. We discuss how the gain of distributed networks may be tuned to enable the behavioral repertoire of these systems, and argue that insect premotor networks might compensate for their limited neuronal population size by, in comparison to vertebrate networks, relying more heavily on the specificity of their connections. At a time in which connectomics and physiological recording techniques enable anatomical and functional circuit dissection at an unprecedented resolution, insect motor systems offer unique opportunities to identify the mechanisms underlying multimodal integration for flexible motor control.