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The Journal of Neurophysiology Vol. 82 No. 2 August 1999, pp. 768-777
Copyright ©1999 by the American Physiological Society
Accumulation Does Not Account for the
Depolarizing Phase of the Synaptic GABA Response in Hippocampal
Pyramidal Cells
Department of Physiology and Pharmacology, State University of New York Health Science Center, Brooklyn, New York 11203
Perkins, Katherine L.
Cl Accumulation Does Not Account for the
Depolarizing Phase of the Synaptic GABA Response in Hippocampal
Pyramidal Cells. J. Neurophysiol. 82: 768-777, 1999. It has been proposed that the depolarizing
phase of the biphasic synaptic GABA response could be mediated by
HCO3
passing through GABAA channels after
dissipation of the transmembrane Cl gradient due to
intracellular Cl accumulation. To test this hypothesis,
giant GABA-mediated postsynaptic currents (GPSCs) were recorded from
pyramidal cells in slices of adult guinea pig hippocampus in the
presence of 4-aminopyridine. GPSCs consisted of an early outward
current (GABAA component) followed by a late inward current
(GABAD component). Spontaneous outward inhibitory
postsynaptic currents (IPSCs) occurred during the GABAD
component of the GPSC. GPSCs that were evoked 1-12 s after the
preceding GPSC (short interval, siGPSCs) showed no GABAD component even though in many cells the amplitude of the siGPSC was
greater than the amplitude of the GABAA component of the
preceding spontaneous GPSC. In addition, the siGPSC evoked during the
GABAD component of a spontaneous GPSC was an outward
current. To test whether the siGPSC lacked a GABAD
component because it was generated predominantly at the soma, where
less of an increase in [Cl]i would occur,
picrotoxin was applied to the soma of the pyramidal cell. To the
contrary, this focal application of picrotoxin caused less of a
reduction in the amplitude of the siGPSC than in the amplitude of the
GABAA component of the GPSC. Furthermore when a GPSC and
siGPSC were evoked 10 s apart using identical stimuli, the area
under the outward current curve was sometimes greater for the siGPSC
than for the GPSC, and yet the siGPSC had no inward component. This
result indicates that even when the location of Cl entry
was the same, more Cl could enter the cell during the
siGPSC than during the outward component of the GPSC and yet not lead
to an inward current. In addition, when the second of two identical
stimuli was applied during the inward GABAD component of
the first evoked GPSC, the GABAA response it generated was
always outward, demonstrating that the equilibrium potential for
GABAA responses did not become more positive than the
holding potential during a GPSC. Finally, evoking GPSCs at a
hyperpolarized potential revealed that the siGPSC actually lacked a
GABAD conductance. These results disprove the
Cl accumulation hypothesis of the synaptic depolarizing
GABA response and suggest the possibility that a separate channel type
may mediate the GABAD component of the GPSC.
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