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The Journal of Neuroscience, August 1, 2000, 20(15):5594-5607
Efficacy and Stability of Quantal GABA Release at a Hippocampal
Interneuron-Principal Neuron Synapse
Udo
Kraushaar and
Peter
Jonas
Physiologisches Institut der Universität Freiburg, D-79104
Freiburg, Germany
We have examined factors that determine the strength and dynamics
of GABAergic synapses between interneurons [dentate gyrus basket cells
(BCs)] and principal neurons [dentate gyrus granule cells (GCs)]
using paired recordings in rat hippocampal slices at 34°C. Unitary
IPSCs recorded from BC-GC pairs in high intracellular Cl concentration showed a fast rise and a
biexponential decay, with mean time constants of 2 and 9 msec. The mean
quantal conductance change, determined directly at reduced
extracellular Ca2+/Mg2+
concentration ratios, was 1.7 nS. Quantal release at the BC-GC synapse
occurred with short delay and was highly synchronized. Analysis of IPSC
peak amplitudes and numbers of failures by multiple probability
compound binomial analysis indicated that synaptic transmission at the
BC-GC synapse involves three to seven release sites, each of which
releases transmitter with high probability (~0.5 in 2 mM
Ca2+/1 mM Mg2+).
Unitary BC-GC IPSCs showed paired-pulse depression (PPD); maximal depression, measured for 10 msec intervals, was 37%, and recovery from
depression occurred with a time constant of 2 sec. Paired-pulse depression was mainly presynaptic in origin but appeared to be independent of previous release. Synaptic transmission at the BC-GC
synapse showed frequency-dependent depression, with half-maximal decrease at 5 Hz after a series of 1000 presynaptic action potentials. The relative stability of transmission at the BC-GC synapse is consistent with a model in which an activity-dependent gating mechanism
reduces release probability and thereby prevents depletion of the
releasable pool of synaptic vesicles. Thus several mechanisms converge
on the generation of powerful and sustained transmission at
interneuron-principal neuron synapses in hippocampal circuits.
Key words:
GABAergic interneurons; basket cells; dentate gyrus; unitary IPSCs; paired-pulse depression; release probability; functional
release sites; vesicular pools; paired recording; multiple probability
compound binomial analysis
Copyright © 2000 Society for Neuroscience 0270-6474/00/20155594-14$05.00/0
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