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Brainstem control of activity and responsiveness in resting frog tadpoles: tonic inhibition

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Abstract

The hatchling Xenopus laevis tadpole was used to study the brain neurons controlling responsiveness. Tadpoles have reduced motor activity and responsiveness when they hang at rest, attached by cement gland mucus. Afferent input from cement gland mechanosensory neurons has both a phasic role in stopping swimming and a tonic role in reducing responsiveness while tadpoles hang attached. Both these roles depend on GABAA-mediated inhibition. We provide evidence supporting the hypothesis that long-term reduced responsiveness in attached tadpoles results from tonic activity in the reticulospinal GABAergic pathway mediating the stopping response. Two groups of putative stopping pathway interneurons were recorded in the caudal and rostral hindbrain of immobilised tadpoles. Both groups showed a sustained increase in activity during simulated attachment. This attached activity was irregular and unstructured. We consider whether low-level firing in cement gland afferents (at ~1 Hz) during simulated attachment is sufficient to explain the low-level firing (at ~0.5 Hz) in reticulospinal neurons. We then ask if a small population of these neurons (~20) could produce sufficient inhibition of spinal neurons to reduce the whole tadpole’s responsiveness. We conclude that for most of their 1st day of life GABAergic brainstem neurons could produce inhibition continuously while the tadpole is at rest.

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Abbreviations

CV:

coefficient of variation

EPSP:

excitatory postsynaptic potential

IPSP:

inhibitory postsynaptic potential

ISI:

interspike interval

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Acknowledgements

We should like to thank Derek Dunn, Julie Hansen and Linda Teagle for technical assistance and Keith Sillar for comments on the manuscript. We are also very grateful to the University of Bristol for providing a postgraduate scholarship to T.D.L. The experiments reported in this paper comply with the Principles of animal care, publication No. 8623, revised 1985 of the National Institutes of Health and with the regulations of the Home Office in the United Kingdom.

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Authors and Affiliations

  1. School of Biological Sciences, University of Bristol, Bristol, UK

    T. D. Lambert, W.-C. Li, S. R. Soffe & A. Roberts

  2. University of Hohenheim, Institute of Physiology, Garbenstrasse 30, 70593, Stuttgart, Germany

    T. D. Lambert

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  1. T. D. Lambert
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  2. W.-C. Li
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  3. S. R. Soffe
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  4. A. Roberts
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Correspondence to T. D. Lambert.

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Lambert, T.D., Li, WC., Soffe, S.R. et al. Brainstem control of activity and responsiveness in resting frog tadpoles: tonic inhibition. J Comp Physiol A 190, 331–342 (2004). https://doi.org/10.1007/s00359-004-0505-8

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  • DOI: https://doi.org/10.1007/s00359-004-0505-8

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