The recurrent case for the Renshaw cell

Bhumbra, G. S., Bannatyne, B. A., Watanabe, M., Todd, A. J. , Maxwell, D. J. and Beato, M. (2014) The recurrent case for the Renshaw cell. Journal of Neuroscience, 34(38), pp. 12919-12932. (doi:10.1523/JNEUROSCI.0199-14.2014) (PMID:25232126) (PMCID:PMC4166169)

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Abstract

Although Renshaw cells (RCs) were discovered over half a century ago, their precise role in recurrent inhibition and ability to modulate motoneuron excitability have yet to be established. Indirect measurements of recurrent inhibition have suggested only a weak modulatory effect but are limited by the lack of observed motoneuron responses to inputs from single RCs. Here we present dual recordings between connected RC–motoneuron pairs, performed on mouse spinal cord. Motoneuron responses demonstrated that Renshaw synapses elicit large inhibitory conductances and show short-term potentiation. Anatomical reconstruction, combined with a novel method of quantal analysis, showed that the strong inhibitory input from RCs results from the large number of synaptic contacts that they make onto individual motoneurons. We used the NEURON simulation environment to construct realistic electrotonic models, which showed that inhibitory conductances from Renshaw inputs exert considerable shunting effects in motoneurons and reduce the frequency of spikes generated by excitatory inputs. This was confirmed experimentally by showing that excitation of a single RC or selective activation of the recurrent inhibitory pathway to generate equivalent inhibitory conductances both suppress motoneuron firing. We conclude that recurrent inhibition is remarkably effective, in that a single action potential from one RC is sufficient to silence a motoneuron. Although our results may differ from previous indirect observations, they underline a need for a reevaluation of the role that RCs perform in one of the first neuronal circuits to be discovered.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Bannatyne, Dr Anne and Todd, Professor Andrew and Maxwell, Professor David
Authors: Bhumbra, G. S., Bannatyne, B. A., Watanabe, M., Todd, A. J., Maxwell, D. J., and Beato, M.
College/School:College of Medical Veterinary and Life Sciences > Institute of Neuroscience and Psychology
Journal Name:Journal of Neuroscience
Publisher:Society for Neuroscience
ISSN:0270-6474
ISSN (Online):1529-2401
Copyright Holders:Copyright © 2014 The Authors
First Published:First published in Journal of Neuroscience 34(38): 12919-12932
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
464671A quantitative description of glycinergic circuits in the ventral horn of the lumbar spinal cord.David MaxwellWellcome Trust (WELLCOME)088279RI NEUROSCIENCE & PSYCHOLOGY
627631Pre-motor neuronal networks, from connectivity to functionDavid MaxwellBiotechnology and Biological Sciences Research Council (BBSRC)BB/L000547/1INP - CENTRE FOR NEUROSCIENCE