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The Journal of Neurophysiology Vol. 82 No. 3 September 1999, pp. 1295-1302
Copyright ©1999 by the American Physiological Society
Neurobiologie et Diversité Cellulaire, Centre National de la Recherche Scientifique Unité Mixte de Recherche 7637, Ecole Supérieure de Physique et de Chimie Industrielles de la ville de Paris, 75231 Paris Cedex 5, France
Angulo, Maria Cecilia,
Jean Rossier, and
Etienne Audinat.
Postsynaptic Glutamate Receptors and Integrative Properties
of Fast-Spiking Interneurons in the Rat Neocortex. J. Neurophysiol. 82: 1295-1302, 1999. The
glutamate-mediated synaptic responses of neocortical pyramidal cell to
fast-spiking interneuron (pyramidal-FS) connections were studied by
performing paired recordings at 30-33°C in acute slices of 14- to
35-day-old rats (n = 39). Postsynaptic fast-spiking (FS) cells were recorded in whole cell configuration with a patch pipette, and presynaptic pyramidal cells were impaled with sharp intracellular electrodes. At a holding potential of 
72 mV (near the
resting membrane potential), unitary excitatory postsynaptic potentials
(EPSPs) had a mean amplitude of 2.1 ± 1.3 mV and a mean width at
half-amplitude of 10.5 ± 3.7 ms (n = 18).
Bath application of the N-methyl-D-aspartate
(NMDA) receptor antagonist D()2-amino-5-phosphonovaleric acid (D-AP5) had minor effects on both the amplitude and
the duration of unitary EPSPs, whereas the
-amino-3-hydroxy-5-methyl-4-isoxazole-propionate (AMPA)/kainate
receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) almost
completely blocked the synaptic responses. In voltage-clamp mode, the
selective antagonist of AMPA receptors
1-(4-aminophenyl)-3-methylcarbamyl-4-methyl-7,8-methylenedioxy-3,4-dihydro-5H-2,3-benzodiazepine (GYKI 53655; 40-66 µM) blocked 96 ± 1.9% of
D-AP5-insensitive unitary excitatory postsynaptic currents
(EPSCs), confirming the predominance of AMPA receptors, as opposed to
kainate receptors, at pyramidal-FS connections (n = 3). Unitary EPSCs mediated by AMPA receptors had fast rise times
(0.29 ± 0.04 ms) and amplitude-weighted decay time constants
(2 ± 0.8 ms; n = 16). In the presence of intracellular spermine, these currents showed the characteristic rectifying current-voltage (I-V) curve of
calcium-permeable AMPA receptors. A slower component mediated by NMDA
receptors was observed when unitary synaptic currents were recorded at
a membrane potential more positive than 50 mV. In response to short
trains of moderately high-frequency (67 Hz) presynaptic action
potentials, we observed only a limited temporal summation of unitary
EPSPs, probably because of the rapid kinetics of AMPA receptors and the
absence of NMDA component in these subthreshold synaptic responses. By
combining paired recordings with extracellular stimulations
(n = 11), we demonstrated that EPSPs elicited by
two different inputs were summed linearly by FS interneurons at
membrane potentials below the action potential threshold. We estimated
that, in our in vitro recording conditions, 8 ± 5 pyramidal cells
(n = 18) should be activated simultaneously to make
FS interneurons fire an action potential from 72 mV. The low level of
temporal summation and the linear summation of excitatory inputs in FS
cells favor the role of coincidence detectors of these interneurons in
neocortical circuits.
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