Locomotor rhythm maintenance: electrical coupling among premotor excitatory interneurons in the brainstem and spinal cord of young Xenopus tadpoles

J Physiol. 2009 Apr 15;587(Pt 8):1677-93. doi: 10.1113/jphysiol.2008.166942. Epub 2009 Feb 16.

Abstract

Electrical coupling is important in rhythm generating systems. We examine its role in circuits controlling locomotion in a simple vertebrate model, the young Xenopus tadpole, where the hindbrain and spinal cord excitatory descending interneurons (dINs) that drive and maintain swimming have been characterised. Using simultaneous paired recordings, we show that most dINs are electrically coupled exclusively to other dINs (DC coupling coefficients approximately 8.5%). The coupling shows typical low-pass filtering. We found no evidence that other swimming central pattern generator (CPG) interneurons are coupled to dINs or to each other. Electrical coupling potentials between dINs appear to contribute to their unusually reliable firing during swimming. To investigate the role of electrical coupling in swimming, we evaluated the specificity of gap junction blockers (18-beta-GA, carbenoxolone, flufenamic acid and heptanol) in paired recordings. 18-beta-GA at 40-60 mum produced substantial (84%) coupling block but few effects on cellular properties. Swimming episodes in 18-beta-GA were significantly shortened (to approximately 2% of control durations). At the same time, dIN firing reliability fell from nearly 100% to 62% of swimming cycles and spike synchronization weakened. Because dINs drive CPG neuron firing and are critical in maintaining swimming, the weakening of dIN activity could account for the effects of 18-beta-GA on swimming. We conclude that electrical coupling among pre motor reticulospinal and spinal dINs, the excitatory interneurons that drive the swimming CPG in the hatchling Xenopus tadpole, may contribute to the maintenance of swimming as well as synchronization of activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Stem / cytology
  • Brain Stem / physiology*
  • Efferent Pathways / cytology
  • Efferent Pathways / physiology*
  • Electrophysiology
  • Gap Junctions / drug effects
  • Gap Junctions / physiology
  • Glycyrrhetinic Acid / analogs & derivatives
  • Glycyrrhetinic Acid / pharmacology
  • Interneurons / drug effects
  • Interneurons / physiology*
  • Interneurons / ultrastructure
  • Larva
  • Locomotion / drug effects
  • Locomotion / physiology*
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Motor Neurons / drug effects
  • Motor Neurons / physiology*
  • Motor Neurons / ultrastructure
  • Patch-Clamp Techniques
  • Spinal Cord / cytology
  • Spinal Cord / physiology*
  • Swimming / physiology
  • Xenopus

Substances

  • 18alpha-glycyrrhetinic acid
  • Glycyrrhetinic Acid