Inhibitory component of the resistance reflex in the locomotor network of the crayfish

J Neurophysiol. 2002 Nov;88(5):2575-88. doi: 10.1152/jn.00178.2002.

Abstract

The aim of this study was to investigate the inhibitory components of a resistance reflex in the walking system of the crayfish. This study was performed using an in vitro preparation of several thoracic ganglia including motor nerves and the proprioceptor that codes movements of the second joint (coxo-basipodite chordotonal organ-CBCO). Sinusoidal movements were imposed on the CBCO, and intracellular responses were recorded from levator (Lev) and depressor (Dep) motoneurons (MNs). We found that in MNs that oppose the imposed movements (e.g., the Lev MNs during the imposed downward movement), the response consists in a depolarization resulting from the summation of excitatory postsynaptic potentials (EPSPs). A movement in the opposite direction resulted in hyperpolarization during which inhibitory postsynaptic potentials (IPSPs) summated. The inhibitory pathway to each MN is oligosynaptic (i.e., composed of a small number of neurons in series) and involves spiking interneurons because it was blocked in the presence of a high-divalent cation solution. The IPSPs were mediated by a chloride conductance because their amplitude was sensitive to the chloride concentration of the bathing solution and because they were blocked by the chloride channel blocker, picrotoxin. Resistance reflex IPSPs related to single CBCO neurons could be identified. These unitary IPSPs were blocked in the presence of 3-mercapto-propionic acid, an inhibitor of gamma-amino-butyric acid (GABA) synthesis, indicating that they are mediated by GABA. In addition to this GABAergic pathway, electrical stimulation of the CBCO sensory nerve induced compound IPSPs that were blocked by glutamate pyruvate transaminase (GPT), indicating the presence of glutamatergic inhibitory pathways. These glutamatergic interneurons do not appear to be involved in the resistance reflex, however, as GPT did not block the unitary IPSPs. Functionally, the resistance reflex is mainly supported by movement-coding CBCO sensory neurons. We demonstrate that such movement-coding CBCO neurons produce both monosynaptic EPSPs in the MNs opposing imposed movements and oligosynaptic IPSPs in the antagonistic motoneurons. These results highlight the similarities between the inhibitory pathways in resistance reflex of the crayfish and in the stretch reflex of vertebrates mediated by Ia inhibitory interneurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astacoidea / physiology*
  • Chloride Channels / drug effects
  • Chloride Channels / physiology
  • Computer Simulation
  • Electrophysiology
  • Excitatory Postsynaptic Potentials / physiology
  • Female
  • GABA Antagonists / pharmacology
  • Glutamic Acid / pharmacology
  • In Vitro Techniques
  • Interneurons / physiology
  • Locomotion / physiology*
  • Male
  • Membrane Potentials / physiology
  • Microelectrodes
  • Microinjections
  • Motor Neurons / physiology*
  • Nerve Net / physiology*
  • Neurotransmitter Agents / physiology
  • Receptors, GABA / drug effects
  • Receptors, GABA / physiology
  • Receptors, Glutamate / drug effects
  • Receptors, Glutamate / physiology
  • Receptors, Neurotransmitter / physiology
  • Reflex / physiology*
  • Walking / physiology*
  • gamma-Aminobutyric Acid / pharmacology

Substances

  • Chloride Channels
  • GABA Antagonists
  • Neurotransmitter Agents
  • Receptors, GABA
  • Receptors, Glutamate
  • Receptors, Neurotransmitter
  • Glutamic Acid
  • gamma-Aminobutyric Acid