Sensory gating of an embryonic zebrafish interneuron during spontaneous motor behaviors.

Laura D Knogler,Pierre Drapeau

doi:10.3389/fncir.2014.00121

Abstract

In all but the simplest monosynaptic reflex arcs, sensory stimuli are encoded by sensory neurons that transmit a signal via sensory interneurons to downstream partners in order to elicit a response. In the embryonic zebrafish (Danio rerio), cutaneous Rohon-Beard (RB) sensory neurons fire in response to mechanical stimuli and excite downstream glutamatergic commissural primary ascending (CoPA) interneurons to produce a flexion response contralateral to the site of stimulus. In the absence of sensory stimuli, zebrafish spinal locomotor circuits are spontaneously active during development due to pacemaker activity resulting in repetitive coiling of the trunk. Self-generated movement must therefore be distinguishable from external stimuli in order to ensure the appropriate activation of touch reflexes. Here, we recorded from CoPAs during spontaneous and evoked fictive motor behaviors in order to examine how responses to self-movement are gated in sensory interneurons. During spontaneous coiling, CoPAs received glycinergic inputs coincident with contralateral flexions that shunted firing for the duration of the coiling event. Shunting inactivation of CoPAs was caused by a slowly deactivating chloride conductance that resulted in lowered membrane resistance and increased action potential threshold. During spontaneous burst swimming, which develops later, CoPAs received glycinergic inputs that arrived in phase with excitation to ipsilateral motoneurons and provided persistent shunting. During a touch stimulus, short latency glutamatergic inputs produced cationic currents through AMPA receptors that drove a single, large amplitude action potential in the CoPA before shunting inhibition began, providing a brief window for the activation of downstream neurons. We compared the properties of CoPAs to those of other spinal neurons and propose that glycinergic signaling onto CoPAs acts as a corollary discharge signal for reflex inhibition during movement.

Highlights

Embryonic circuits must be capable of responding to sensory stimuli in order to perform essential motor behaviors such as avoiding predation
In embryos ≥26 hpf, commissural primary ascending (CoPA) produced sustained firing throughout the duration of the current step and less current was needed to bring the neuron to threshold (Figure 1A; N = 9/9)
We examined the sensitivity of these receptors to external polyamine block by applying 10 μM philanthotoxin 343 (PhTX) to our recordings of AMPAergic mEPSCs from CoPAs

Summary

Introduction

Embryonic circuits must be capable of responding to sensory stimuli in order to perform essential motor behaviors such as avoiding predation. Sensorimotor circuits must be organized in such a way that the animal’s own movement is distinguishable from movement in the environment in order to make computations regarding expected and novel sensory feedback. One way in which the nervous system compensates for self-movement is to send corollary discharge signals from motorrelated pathways to modulate activation of sensory pathways (reviewed by Crapse and Sommer, 2008). Corollary discharges may target different parts of the sensory pathway and use diverse mechanisms to alter sensory function depending on the species and the modality being studied. The embryonic vertebrate spinal cord provides a simplified neural network within which to study the modulation of sensory pathways that ensure the appropriate activation of sensorimotor behaviors. Following a touch to the skin, one or more Rohon-Beard (RB)

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