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Journal of Neuroscience, Vol 14, 4433-4445, Copyright © 1994 by Society for Neuroscience
Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission
CJ McBain, TJ DiChiara and JA Kauer
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710.
Based on responses to metabotropic glutamate receptor (mGluR) activation,
we have characterized two distinct classes of interneuron in stratum (st.)
oriens of the CA1 region of hippocampus. One type of interneuron was
strongly excited by 1S,3R-aminocyclopentane dicarboxylic acid (ACPD),
responding with a large inward current accompanied by increased baseline
noise and prominent current oscillations. A second interneuron population
responded with a modest inward current with no changes in baseline noise.
These two classes of responses persisted in the presence of tetrodotoxin
and antagonists of ionotropic glutamate and GABA receptors, suggesting that
the inward currents result from mGluRs on the interneurons themselves. The
two physiologically defined cell types correspond to two distinct
morphological cell types in st. oriens/alveus, distinguished by very
different patterns of local axonal connections. Large oscillatory inward
current responses were recorded predominantly from an interneuron type
whose axons heavily innervated st. lacunosum. The more modest inward
current response was generally found in interneurons whose axons innervated
the somata and proximal dendrites of CA1 pyramidal neurons. These
differences in physiology and local circuitry imply that activation of
mGluRs in st. oriens will cause very strong excitation of interneurons
synapsing in st. lacunosum, and weaker excitation of interneurons
innervating pyramidal cells at the soma and proximal dendrites. These data
suggest that each interneuron population has a specific role in hippocampal
function, and that mGluR activation will affect the local circuit
differently for each interneuron type. Metabotropic GluR activation also
markedly enhanced the amplitudes of the evoked and spontaneous EPSCs
received by all interneurons in the region, independent of changes in the
postsynaptic holding current and with no change in the kinetics of the
EPSC. In contrast to the enhancement of evoked and spontaneous EPSCs,
miniature EPSCs recorded in the presence of tetrodotoxin were not
increased. These data suggest that ACPD acts at a presynaptic site to
potentiate the EPSC. Taken together, these results highlight an important
modulatory role for metabotropic receptors located at sites both pre- and
postsynaptic to CA1 st. oriens interneurons.
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