Spinal corollary discharge modulates motion sensing during vertebrate locomotion.

Boris P Chagnaud,Hans Straka,John Simmers,Roberto Banchi

doi:10.1038/ncomms8982

Abstract

During active movements, neural replicas of the underlying motor commands may assist in adapting motion-detecting sensory systems to an animal's own behaviour. The transmission of such motor efference copies to the mechanosensory periphery offers a potential predictive substrate for diminishing sensory responsiveness to self-motion during vertebrate locomotion. Here, using semi-isolated in vitro preparations of larval Xenopus, we demonstrate that shared efferent neural pathways to hair cells of vestibular endorgans and lateral line neuromasts express cyclic impulse bursts during swimming that are directly driven by spinal locomotor circuitry. Despite common efferent innervation and discharge patterns, afferent signal encoding at the two mechanosensory peripheries is influenced differentially by efference copy signals, reflecting the different organization of body/water motion-detecting processes in the vestibular and lateral line systems. The resultant overall gain reduction in sensory signal encoding in both cases, which likely prevents overstimulation, constitutes an adjustment to increased stimulus magnitudes during locomotion.

Highlights

During active movements, neural replicas of the underlying motor commands may assist in adapting motion-detecting sensory systems to an animal’s own behaviour
Following a short tonic firing at swim episode onset, the two vestibular nerve branches displayed sustained rhythmic discharge that was closely timed with spinal vr motor bursting on the same side of the cord
The strict in-phase coordination of anterior vestibular nerve (AVN) and PVN discharge with ipsilateral vr burst activity and their out-of-phase relationship with contralateral vr bursts was confirmed by circular plot analysis of instantaneous vr firing relative to spiking in both vestibular nerves recorded on the same side (PVN, blue and AVN, red in Fig. 1f; Supplementary Fig. 1d,e)

Summary

Introduction

Neural replicas of the underlying motor commands may assist in adapting motion-detecting sensory systems to an animal’s own behaviour. Despite common efferent innervation and discharge patterns, afferent signal encoding at the two mechanosensory peripheries is influenced differentially by efference copy signals, reflecting the different organization of body/water motion-detecting processes in the vestibular and lateral line systems. In contrast to reactive sensory-derived processes, the predictive nature of these intrinsic feed-forward signals is well suited to inform associated sensory systems at various levels of the nervous system about impending and/or ongoing motor activity[7,8,9,10] In this context, vertebrates possess a highly suitable neuronal substrate for a peripheral gain control mechanism that can tune hair cell sensitivity and adapt afferent encoding in the movement-detecting periphery of both the vestibular and lateral line sensory systems[11,12]. Despite some evidence for a behavioural context-specific role, a general functional picture of these efferent systems and their impact on mechano-afferent encoding has so far remained elusive

Methods

Results

Conclusion