A glycine receptor is involved in the organization of swimming movements in an invertebrate chordate.

Atsuo Nishino,Yasushi Okamura,Stefania Piscopo,Euan R Brown

doi:10.1186/1471-2202-11-6

Abstract

BackgroundRhythmic motor patterns for locomotion in vertebrates are generated in spinal cord neural networks known as spinal Central Pattern Generators (CPGs). A key element in pattern generation is the role of glycinergic synaptic transmission by interneurons that cross the cord midline and inhibit contralaterally-located excitatory neurons. The glycinergic inhibitory drive permits alternating and precisely timed motor output during locomotion such as walking or swimming. To understand better the evolution of this system we examined the physiology of the neural network controlling swimming in an invertebrate chordate relative of vertebrates, the ascidian larva Ciona intestinalis.ResultsA reduced preparation of the larva consisting of nerve cord and motor ganglion generates alternating swimming movements. Pharmacological and genetic manipulation of glycine receptors shows that they are implicated in the control of these locomotory movements. Morphological molecular techniques and heterologous expression experiments revealed that glycine receptors are inhibitory and are present on both motoneurones and locomotory muscle while putative glycinergic interneurons were identified in the nerve cord by labeling with an anti-glycine antibody.ConclusionsIn Ciona intestinalis, glycine receptors, glycinergic transmission and putative glycinergic interneurons, have a key role in coordinating swimming movements through a simple CPG that is present in the motor ganglion and nerve cord. Thus, the strong association between glycine receptors and vertebrate locomotory networks may now be extended to include the phylum chordata. The results suggest that the basic network for 'spinal-like' locomotion is likely to have existed in the common ancestor of extant chordates some 650 M years ago.

Highlights

Rhythmic motor patterns for locomotion in vertebrates are generated in spinal cord neural networks known as spinal Central Pattern Generators (CPGs)
Physiology, pharmacology and phylogeny of locomotion One of the main roles of the nervous system in the ascidian larva is to generate swimming movements that are manifested in alternating tail beats that occur between 10-40 Hz
Our microdissection experiments confirm the role of the motor ganglion (MG) in controlling and generating motor patterns, as ‘headless’ larvae lacking both otolith and ocellus, but with tail and MG intact, are capable of coordinated swimming movements when L-glutamate is added to the bath

Summary

Introduction

Rhythmic motor patterns for locomotion in vertebrates are generated in spinal cord neural networks known as spinal Central Pattern Generators (CPGs). To understand better the evolution of this system we examined the physiology of the neural network controlling swimming in an invertebrate chordate relative of vertebrates, the ascidian larva Ciona intestinalis. Intracellular recording from muscle cells from two distantly spaced electrodes shows near-simultaneous activation of the muscles on one side of the tail during swimming strokes [9] This means that the traveling wave that is generated is due to the interaction of the muscle, notochord and resistive forces with the surrounding fluid and not because of sequential activation of segmented muscle cells as in vertebrates. The travelling wave during swimming is produced by sequential activation of coupled spinal networks acting on segmented muscle Despite these fundamental differences, here we find that the contribution of glycinergic inhibitory transmission is a common feature in both vertebrate and non-vertebrate chordate locomotory control

Results

Discussion

Conclusion