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Open Access Highly Accessed Research article

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

Atsuo Nishino12, Yasushi Okamura23, Stefania Piscopo4 and Euan R Brown4*

Author Affiliations

1 Department of Biological Sciences, Graduate School of Science, Osaka University, Machikaneyama 1-1, Toyonaka, Osaka 560-0043, Japan

2 Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences, Higashiyama 5-1, Myodaiji, Okazaki, Aichi 444-8787, Japan

3 Department of Integrative Physiology, Graduate School of Medicine, Osaka University, Yamada-Oka 2-2, Suita, Osaka, 565-0871, Japan

4 Laboratorio di Fisiologia Animale ed Evoluzione, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italia

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BMC Neuroscience 2010, 11:6  doi:10.1186/1471-2202-11-6

Published: 19 January 2010

Abstract

Background

Rhythmic 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.

Results

A 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.

Conclusions

In 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.