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Journal of Neuroscience, Vol 14, 2365-2376, Copyright © 1994 by Society for Neuroscience
Patch-clamp recordings reveal powerful GABAergic inhibition in dentate hilar neurons
I Soltesz and I Mody
Department of Anesthesiology, and Pain Management, UT Southwestern Medical Center, Dallas 75235-9068.
Whole-cell and cell-attached patch-clamp recordings were used to
investigate the nature of GABAA receptor-mediated inhibition in the adult
rat dentate gyrus in standard 400-microns-thick horizontal slices. In the
presence of the glutamate receptor antagonists D-2-amino-
5-phosphonovaleric acid and 6-cyano-7-nitroquinoxaline-2,3-dione, whole-
cell voltage-clamp experiments with chloride-filled electrodes ([Cl-]in =
[Cl-]out) revealed a high degree of spontaneous activity (10-60 Hz) in all
hilar neurons (HNs) recorded with access resistances lower than 20 M omega.
The events were inward at negative holding potentials, reversed at around
the Cl- equilibrium potential, and were completely abolished by the
specific antagonists of the GABAA receptor channel picrotoxin and SR-95531
in a reversible manner, indicating that they were spontaneous inhibitory
postsynaptic currents (sIPSCs) mediated by GABAA receptors. The majority of
the sIPSCs were TTX-insensitive miniature currents resulting from the
action potential-independent release of GABA. The 10-90% rise times and the
monoexponential decay time constants of the sIPSCs were significantly
longer in HNs than those found in neighboring granule cells (GCs).
Furthermore, the decay time constant of the hilar sIPSCs was not voltage
dependent, contrary to the voltage dependency of the decay time constant of
the sIPSCs recorded from GCs. As HNs have longer electrotonic length than
GCs do, dendritic filtering may contribute to the kinetic differences. Non-
stationary fluctuation analysis showed that whereas the number of channels
open at the peak of individual sIPSCs was similar, the single- channel
conductances significantly differed between the two cell groups. The 21%
smaller single-channel conductance and the existence of electrotonically
close GABAergic synapses on HNs indicate that dendritic filtering alone
cannot explain the differences between HNs and GCs. The distinct subunit
composition of the GABAA receptor channels in HNs and GCs may also be
responsible for the altered kinetics of IPSCs in HNs. However, the subunit
specific benzodiazepine agonist zolpidem (3 microns) prolonged the
monoexponential decay time constants in both HNs and GCs. Thus, differences
between the GABAA receptors of the two cell types are not due to a simple
all-or-none presence/absence of the alpha 5 subunit.(ABSTRACT TRUNCATED AT
400 WORDS)
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