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The neuronal targets for GABAergic reticulospinal inhibition that stops swimming in hatchling frog tadpoles

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Abstract

In most animals locomotion can be started and stopped by specific sensory cues. We are using a simple vertebrate, the hatchling Xenopus tadpole, to study a neuronal pathway that turns off locomotion. In the tadpole, swimming stops when the head contacts solid objects or the water's surface meniscus. The primary sensory neurons are in the trigeminal ganglion and directly excite inhibitory reticulospinal neurons in the hindbrain. These project axons into the spinal cord and release GABA to inhibit spinal neurons and stop swimming. We ask whether there is specificity in the types of spinal neuron inhibited. We used single-neuron recording to determine which classes of spinal neurons receive inhibition when the head skin is pressed. Ventral motoneurons and premotor interneurons involved in generating the swimming rhythm receive reliable GABAergic inhibition. More dorsal inhibitory premotor interneurons are inhibited less reliably and some are excited. Dorsal sensory pathway interneurons that start swimming following a touch to the trunk skin do not appear to receive such inhibition. There is therefore specificity in the formation of descending inhibitory connections so that more ventral neurons producing swimming are most strongly inhibited.

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Abbreviations

aIN :

ascending interneuron

cIN :

commissural interneuron

CPG :

central pattern generator

dIN :

descending interneuron

dlc :

dorsolateral commissural interneuron

EPSP :

excitatory post-synaptic potential

MHR :

midhindbrain reticulospinal interneuron

Pl-W :

pleural withdrawal neuron

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Acknowledgements

We should like to thank Derek Dunn, Julie Hansen and Linda Teagle for technical assistance, and Steve Soffe for advice and comments on the manuscript. Supported by the Wellcome Trust. The experiments reported in this paper comply with the National Institute of Health Principles of Animal Care, publication No. 86-23, revised 1985, and with the regulations of the Home Office in the United Kingdom.

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Correspondence to A. Roberts.

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Li, WC., Perrins, R., Walford, A. et al. The neuronal targets for GABAergic reticulospinal inhibition that stops swimming in hatchling frog tadpoles. J Comp Physiol A 189, 29–37 (2003). https://doi.org/10.1007/s00359-002-0372-0

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  • DOI: https://doi.org/10.1007/s00359-002-0372-0

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