Phase‐dependent Modulation of a Cutaneous Sensory Pathway by Glycinergic Inhibition from the Locomotor Rhythm Generator in Xenopus Embryos

Keith T. Sillar*, Alan Roberts

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

In immobilized Xenopus laevis embryos two classes of sensory interneuron are excited by mechanosensory Rohon‐Beard neurons and rhythmically inhibited during fictive swimming. Dorsolateral commissural (DLC) interneurons are inhibited in time with rhythmic motor discharge on the same side as their soma, while unidentified dorsolateral (DLX) interneurons are inhibited in the opposite phase of the swimming rhythm. The inhibition is abolished by bath application of strychnine sulphate at 1–10 μM, but not by the γ‐aminobutyric acid antagonists bicuculline (20–40 μM) or curare (70–100 μM). The inhibitory postsynaptic potentials (IPSPs) involve an increase in chloride conductance since they are reversed in sign to become depolarizing following intracellular injection of chloride ions. The conductance increase during inhibition was able to block impulses evoked by intracellular current in a phase‐dependent manner, suggesting that postsynaptic inhibition is sufficient to account for the gating of afferent input to the spinal cord during swimming. An interneuron receives IPSPs that are predominantly in one phase of the rhythm, but most interneurons are also inhibited sporadically in the opposite phase. The amplitude and time course of the IPSPs closely follow the frequency of the swimming rhythm, with maximal inhibition occurring near the starts of episodes, when swimming frequency is at its highest. Towards the end of an episode, when swimming frequency declines, the level of inhibition is low, the membrane potential of the interneurons returns to rest between cycles, and IPSPs often fail to occur. Inhibition suppresses sensory excitation in a phase‐dependent manner (cf. Sillar and Roberts, Nature, 331, 262–265, 1988). Sensory interneurons fire a single impulse in response to a brief sensory stimulus, but they will usually fire multiple impulses when depolarized with sufficient intracellular current. In some sensory interneurons a short‐latency IPSP follows the impulse evoked by skin stimulation that could curtail impulse activity. However, when the inhibition is blocked by strychnine, sensory interneurons still fire a single short‐latency impulse, favouring the conclusion that brief, synchronized afferent excitation elicits a single impulse in neurons that are capable of firing multiply. Since the inhibition of DLC interneurons occurs in phase with activity on the same side it probably originates from spiking in ipsilateral glycinergic commissural interneurons which have ipsilateral as well as contralateral projections. The inhibition of DLX interneurons in the opposite phase probably originates from the contralateral projections of commissural interneurons.

Original languageEnglish
Pages (from-to)1022-1034
Number of pages13
JournalEuropean Journal of Neuroscience
Volume4
Issue number11
DOIs
Publication statusPublished - Nov 1992

Keywords

  • glycine
  • inhibition
  • interneuron
  • locomotion
  • modulation
  • spinal cord

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