Activation of interneurons at the stratum oriens/alveus border suppresses excitatory transmission to apical dendrites in the CA1 area of the mouse hippocampus

Y. Yanovsky, O. A. Sergeeva, T. F. Freund, H. L. Haas

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Abstract

The consequences of activation or inactivation of interneurons at the CA1 stratum oriens/alveus border for signal transmission at the apical dendritic region of pyramidal cells were investigated in slices from mice submerged in a perfusion chamber. A characteristic subpopulation of interneurons with a horizontal dendritic tree in this region, which sends a GABAergic projection to the apical dendrites of CA1 pyramidal cells is strongly excited by metabotropic glutamate receptor activation and receives GABAergic input from vasoactive intestinal polypeptide-containing interneurons. Pressure ejection of glutamate or the metabotropic agonist 1s,3r-aminocyclopentane dicarboxylic acid from micropipettes onto the stratum oriens/alveus border caused a long lasting (more than 90 min) decrease of field-excitatory postsynaptic potentials in the strata radiatum and lacunosum-moleculare. The GABA(B) antagonist CGP 35348 (100 μM in the perfusion fluid) partially and reversibly blocked this effect. Vasoactive intestinal polypeptide- (0.1 μM in the bath) excited neurons with response and firing properties characteristic for interneurons at the oriens/alveus border. Local pressure application of vasoactive intestinal polypeptide (10 μM) to the alveus region led, after a brief (2 min) and small (10%) increase, to a longer lasting (30-50 min) decrease (by 20-30%) in the slope of the field-excitatory postsynaptic potential in strata radiatum and lacunosum-moleculare. This action was completely blocked by bath application of CGP 35348. Local application of tetrodotoxin in the stratum oriens/alveus region markedly increased the slope of evoked dendritic excitatory postsynaptic potentials, and caused multiple firing of pyramidal cells. Thus, stratum oriens/alveus interneurons have a profound inhibitory effect on signal transmission in the apical dendritic area of CA1, which is, at least in part, mediated by GABA(B) receptors. It appears that the GABA(B) receptor-mediated effect in stratum lacunosum-moleculare is produced by vasoactive intestinal polypeptide-sensitive interneurons.

Original languageEnglish
Pages (from-to)87-96
Number of pages10
JournalNeuroscience
Volume77
Issue number1
DOIs
Publication statusPublished - Jan 6 1997

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Keywords

  • GABA
  • Glutamate
  • Inhibition
  • Metabotropic receptors
  • VIP

ASJC Scopus subject areas

  • Neuroscience(all)

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