Development and role of GABA(A) receptor-mediated synaptic potentials during swimming in postembryonic Xenopus laevis tadpoles.
We have investigated the contribution of GABA(A) receptor activation to swimming in Xenopus tadpoles during the first day of postembryonic development. Around the time of hatching stage (37/8), bicuculline (10-50 microM) causes a decrease in swim episode duration and cycle period, suggesting that GABA(A) receptor activation influences embryonic swimming. Twenty-four hours later, at stage 42, GABA(A) receptor activation plays a more pronounced role in modulating larval swimming activity. Bicuculline causes short, intense swim episodes with increased burst durations and decreased cycle periods and rostrocaudal delays. Conversely, the allosteric agonist, 5beta-pregnan-3alpha-ol-20-one (1-10 microM) or the uptake inhibitor, nipecotic acid (200 microM) cause slow swimming with reduced burst durations and increased cycle periods. These effects appear to be mainly the result of GABA release from the spinal terminals of midhindbrain reticulospinal neurons but may also involve spinal GABAergic neurons. Intracellular recordings were made using KCl electrodes to reverse the sign and enhance the amplitude of chloride-dependent inhibitory postsynaptic potentials (IPSPs). Recordings from larval motoneurons in the presence of strychnine (1-5 microM), to block glycinergic IPSPs, provided no evidence for any GABAergic component to midcycle inhibition. GABA potentials were observed during episodes, but they were not phase-locked to the swimming rhythm. Bicuculline (10-50 microM) abolished these sporadic potentials and caused an apparent decrease in the level of tonic depolarization during swimming activity and an increase in spike height. Finally, in most larval preparations, GABA potentials were observed at the termination of swimming. In combination with the other evidence, our data suggest that midhindbrain reticulospinal neurons become involved in an intrinsic pathway that can prematurely terminate swim episodes. Thus during the first day of larval development, endogenous activation of GABA(A) receptors plays an increasingly important role in modulating locomotion, and GABAergic neurons become involved in an intrinsic descending pathway for terminating swim episodes.
Reith
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School of Biology, Gatty Marine Laboratory, University of St. Andrews, St. Andrews, Fife KY16 8LB, Scotland.
Sillar
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D000818:Animals; D001640:Bicuculline / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D018757:GABA Modulators / Q000494:pharmacology; D018684:Glycine Agents / Q000494:pharmacology; D007814:Larva; D009474:Neurons / Q000502:physiology; D009557:Nipecotic Acids / Q000494:pharmacology; D011280:Pregnanolone / Q000494:pharmacology; D011392:Proline / Q000031:analogs & derivatives*; D011963:Receptors, GABA-A / Q000187:drug effects / Q000502:physiology*; D012249:Rhombencephalon / Q000166:cytology / Q000502:physiology; D013116:Spinal Cord / Q000166:cytology / Q000502:physiology; D013331:Strychnine / Q000494:pharmacology; D013550:Swimming / Q000502:physiology*; D013569:Synapses / Q000187:drug effects / Q000502:physiology*; D014982:Xenopus laevis; D005680:gamma-Aminobutyric Acid / Q000502:physiology
D018756:GABA Antagonists; D018757:GABA Modulators; D018684:Glycine Agents; D009557:Nipecotic Acids; D011963:Receptors, GABA-A; C030278:nipecotic acid; D005680:gamma-Aminobutyric Acid; D011392:Proline; D011280:Pregnanolone; C010983:homoproline; D013331:Strychnine; D001640:Bicuculline