Metabotropic glutamate receptors and blockade of glial Krebs cycle depress glycinergic synaptic currents of mouse hypoglossal motoneurons

Eur J Neurosci. 2000 Jan;12(1):239-46. doi: 10.1046/j.1460-9568.2000.00902.x.

Abstract

Metabotropic glutamate receptors are known to depress synaptic transmission by inhibiting transmitter release from presynaptic nerve terminals. This study reports the effects of presynaptic metabotropic glutamate receptor activation on inhibitory synaptic transmission in hypoglossal motoneurons in brainstem slice preparations of neonatal mice. Whole-cell patch-clamp recordings were performed on hypoglossal motoneurons of 2-6-day-old mice. Monosynaptic glycinergic currents were elicited by electrical stimulation of the nucleus of Roller. Application of the specific metabotropic glutamate receptor agonists (+/-)-1-aminocyclopentane-trans-1,3,dicarboxylic acid (t-ACPD), (2S, 2'R,3'R)-2-(2',3'-dicarboxylcyclopropyl)-glycine (DCG-IV) or L-2-amino-4-phosphonobutyric acid (L-AP4) depressed stimulus-evoked glycinergic inhibitory postsynaptic currents (IPSCs) by an average of 39.5, 59.4 and 39.2%, respectively. In the presence of t-ACPD, glycinergic miniature IPSCs were reduced in frequency but not in amplitude, which is indicative of a presynaptic mechanism. A similar reduction of IPSC amplitude was observed in the presence of elevated extracellular glutamate or during application of D, L-threo-hydroxyaspartate (THA), a blocker of glutamate transport, respectively. The data suggest that uptake of glutamate, which is predominately carried out by glial cells, can prevent spill-over of glutamate and activation of metabotropic glutamate receptors. A reduction of IPSCs was also observed following application of monofluoroacetic acid, a substance acting specifically on glial cells. Our results suggest that glial regulation of extracellular glutamate uptake can prevent spill-over of glutamate, and glutamatergic depression of glycinergic inhibition in hypoglossal motoneurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Aspartic Acid / analogs & derivatives
  • Aspartic Acid / pharmacology
  • Citric Acid Cycle*
  • Cycloleucine / analogs & derivatives
  • Cycloleucine / pharmacology
  • Cyclopropanes / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology*
  • Female
  • Glycine / analogs & derivatives
  • Glycine / pharmacology
  • Glycine / physiology
  • Hypoglossal Nerve / physiology*
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Methoxyhydroxyphenylglycol / analogs & derivatives
  • Methoxyhydroxyphenylglycol / pharmacology
  • Mice
  • Mice, Inbred Strains
  • Motor Neurons / physiology*
  • Neuroglia / physiology*
  • Neuroprotective Agents / pharmacology
  • Patch-Clamp Techniques
  • Propionates / pharmacology
  • Receptors, Metabotropic Glutamate / agonists
  • Receptors, Metabotropic Glutamate / antagonists & inhibitors
  • Receptors, Metabotropic Glutamate / physiology*
  • Synapses / physiology*

Substances

  • 2-amino-4-phosphono-propinate
  • Cyclopropanes
  • Neuroprotective Agents
  • Propionates
  • Receptors, Metabotropic Glutamate
  • Cycloleucine
  • 1-amino-1,3-dicarboxycyclopentane
  • 2-(2,3-dicarboxycyclopropyl)glycine
  • 3-hydroxyaspartic acid
  • Aspartic Acid
  • Methoxyhydroxyphenylglycol
  • Glycine
  • 3,4-dihydroxyphenylglycol