A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons

Département de Physiologie, Centre de Recherche en Sciences Neurologiques, Université de Montréal, Case Postale 6128, Succursale Centre-ville, Montréal, QC, Canada H3C 3J7

Edited by Per O. Andersen, University of Oslo, Oslo, Norway, and approved June 5, 2001 (received for review October 17, 2000)

Abstract

Hippocampal inhibitory interneurons play important roles in controlling the excitability and synchronization of pyramidal cells, but whether they express long-term synaptic plasticity that contributes to hippocampal network function remains uncertain. We found that pairing postsynaptic depolarization with θ-burst stimulation induced long-term potentiation (LTP) of putative single-fiber excitatory postsynaptic currents in interneurons. Either postsynaptic depolarization or θ-burst stimulation alone failed to induce LTP. LTP was expressed as a decrease in failure rates and an increase in excitatory postsynaptic current amplitude, independent of N-methyl-d-aspartate receptors, and dependent on metabotropic glutamate receptors subtype 1a. LTP was induced specifically in interneurons in stratum oriens and not in interneurons of stratum radiatum/lacunosum-moleculare. Thus, excitatory synapses onto specific subtypes of inhibitory interneurons express a new form of hebbian LTP that will contribute to hippocampal network plasticity.

Footnotes

↵ * To whom reprint requests should be addressed. E-mail: jean-claude.lacaille{at}umontreal.ca.
This paper was submitted directly (Track II) to the PNAS office.
↵ † Gee, C. & Lacaille, J.-C. (2000) Soc. Neurosci. Abstr. 26, 2342.
Abbreviations:

LTP,

long-term potentiation;

EPSC,

excitatory postsynaptic current;

NMDAR,

N-methyl-d-aspartate receptor;

ACSF,

artificial cerebrospinal fluid;

AP5,

dl-2-amino-5-phosphonopentanoic acid;

E4CPG,

(RS)-α-ethyl-4-carboxyphenylglycine;

MCPG,

(RS)-α-methyl-4-carboxyphenylglycine;

LY367385,

(+)-2-methyl-4-carboxyphenylglycine;

TBS,

θ-burst stimulation;

rmANOVA,

repeated measures ANOVA;

AMPA,

α-amino-3-hydroxy-5-methyl-4-isoxazole-propionate;

KA,

kainate;

mGluR,

metabotropic glutamate receptor;

R/LM,

stratum radiatum near lacunosum-moleculare;

NHPP,

N-(4-hydroxyphenylpropanoyl)spermine