Nitric oxide selectively tunes inhibitory synapses to modulate vertebrate locomotion

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Abstract

We have explored the possible modulation by nitric oxide (NO) of inhibitory synaptic transmission mediated by either glycine or GABA during episodes of rhythmic fictive swimming in postembryonic Xenopus laevis tadpoles. Extracellular ventral-root recordings suggest a stage-dependent increase in the reliability and extent of the NO donor S-nitroso-n-acetylpenicillamine (SNAP; 0.1-1 mM) to inhibit swimming by reducing the frequency and shortening the duration of swim episodes. These effects of SNAP on the swimming rhythm at both developmental stages are corroborated by intracellular recordings from presumed motor neurons with sharp microelectrodes, which also suggest that NO inhibits swimming by facilitating both glycinergic and GABAergic inhibition. However, we found no evidence for NO modulation of the excitatory drive for swimming. In addition to presynaptic effects on inhibitory transmitter release, a pronounced postsynaptic membrane depolarization (similar to5-10 mV) and conductance decrease (similar to10-20%) are associated with bath application of SNAP. Hence, NO exerts inhibitory effects on swimming through multiple but selective actions on both the electrical properties of spinal neurons and on particular synaptic interconnections. The presynaptic and postsynaptic effects of NO act in concert to tune inhibitory synapses.

Original languageEnglish
Pages (from-to)4175-4184
Number of pages10
JournalThe Journal of Neuroscience
Volume22
Issue number10
Publication statusPublished - 15 May 2002

Keywords

  • nitric oxide
  • GABA
  • glycine
  • spinal cord
  • release
  • locomotion
  • XENOPUS-LAEVIS EMBRYOS
  • POSTEMBRYONIC DEVELOPMENT
  • STOPPING RESPONSE
  • PATTERN GENERATOR
  • SPINAL NEURONS
  • NERVOUS-SYSTEM
  • MOTOR PATTERN
  • BRAIN-STEM
  • CHANNELS
  • TADPOLES

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