Local effects of glycinergic inhibition in the spinal cord motor systems for swimming in amphibian embryos

J Neurophysiol. 1996 Aug;76(2):1025-35. doi: 10.1152/jn.1996.76.2.1025.

Abstract

1. We have studied the effects of locally applying the glycinergic antagonist strychnine to rhythmically active spinal neurons in amphibian embryos during fictive swimming. Intracellular recordings were made from motoneurons and premotor interneurons in Xenopus laevis, a well-studied model system, and from motoneurons in three other species (Rana temporaria, Bufo bufo, and Triturus vulgaris). Overall, these embryos cover a range of swimming patterns from the short-cycle-period, brief-motor-root bursts of Xenopus, to the long-cycle-period, long-motor-root bursts of Rana, which are more typical of adult patterns. 2. Local strychnine application had no significant effect on the gross pattern of swimming; episode duration and the burst duration in rostral ventral roots away from the application site were unaltered, and left-right alternation was preserved. We have therefore been able to examine the effects of inhibition on individual neurons, uninfluenced by overall changes in the operation of the swimming neural circuitry. 3. In all cases strychnine blocked midcycle inhibition and significantly increased the peak on-cycle depolarization during swimming. In Rana, Bufo, and Triturus motoneurons, and in Xenopus interneurons, strychnine significantly increased the reliability of firing during swimming. In Xenopus motoneurons, where spiking was 100% reliable anyway, the timing of the spikes was advanced relative to rostral ventral root activity. These results do not provide support for postinhibitory rebound as a factor in the spike-generating process during swimming. In addition to midcycle inhibition, Xenopus motoneurons can also show a smaller, additional on-cycle inhibition that is blocked by strychnine. 4. In both Rana and Bufo the duration of caudal ventral root bursts close to the site of drug application was increased by strychnine, showing that the increased motoneuron reliability not only leads to more intense, but also more extensive, ventral root activity. 5. At the level of single neurons, glycinergic inhibition effectively reduces on-cycle excitation and in turn controls the reliability, extent, and precise timing of motoneuron firing. These changes may be the individual components underlying broader effects of inhibition described previously, such as locomotor frequency control. They also show how any modulation of inhibition in localized regions of the spinal cord could produce localized control of neuronal firing properties.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amphibians / embryology
  • Amphibians / physiology*
  • Animals
  • Embryo, Nonmammalian
  • Glycine Agents / administration & dosage
  • Glycine Agents / pharmacology
  • Interneurons / drug effects
  • Interneurons / physiology
  • Microinjections
  • Motor Neurons / drug effects
  • Motor Neurons / physiology
  • Receptors, Glycine / antagonists & inhibitors
  • Receptors, Glycine / physiology*
  • Spinal Cord / cytology
  • Spinal Cord / drug effects
  • Spinal Cord / physiology*
  • Strychnine / administration & dosage
  • Strychnine / pharmacology
  • Swimming / physiology

Substances

  • Glycine Agents
  • Receptors, Glycine
  • Strychnine