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The Journal of Neuroscience, November 29, 2006, 26(48):12487-12496; doi:10.1523/JNEUROSCI.3106-06.2006
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Cellular/Molecular
Release Probability-Dependent Scaling of the Postsynaptic Responses at Single Hippocampal GABAergic Synapses
Ágota A. Biró, * Noémi B. Holderith, * andZoltan Nusser Laboratory of Cellular Neurophysiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083 Budapest, Hungary
Correspondence should be addressed to Zoltan Nusser, Laboratory of Cellular Neurophysiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony Street 43, 1083 Budapest, Hungary. Email: nusser{at}koki.hu
The amount of neurotransmitter released after the arrival of an action potential affects the strength and the trial-to-trial variability of postsynaptic responses. Most studies examining the dependence of synaptic neurotransmitter concentration on the release probability (Pr) have focused on glutamatergic synapses. Here we asked whether univesicular or multivesicular release characterizes transmission at hippocampal GABAergic synapses. We used multiple probability functional analysis to derive quantal parameters at inhibitory connections between cannabinoid receptor- and cholecystokinin (CCK)-expressing interneurons and CA3 pyramidal cells. After the recordings, the cells were visualized and reconstructed at the light-microscopic level, and the number of boutons mediating the IPSCs was determined using electron microscopy (EM). The number of active zones (AZs) per CCK-immunopositive bouton was determined from three-dimensional EM reconstructions, thus allowing the calculation of the total number of AZs for each pair. Our results reveal an approximate fivefold discrepancy between the numbers of functionally determined release sites (17.4 ± 3.2) and structurally identified AZs (3.7 ± 0.9). Channel modeling predicts that a fivefold to sevenfold increase in the peak synaptic GABA concentration is required for the fivefold enhancement of the postsynaptic responses. Kinetic analysis of the unitary IPSCs indicates that the increase in synaptic GABA concentration is most likely attributable to multivesicular release. This change in the synaptic GABA concentration transient together with extremely low postsynaptic receptor occupancy permits a Pr-dependent scaling of the postsynaptic response generated at a single hippocampal GABAergic synaptic contact.
Key words: patch clamp; paired recordings; electron microscopy; quantal analysis; hippocampus; interneurons
Received July 21, 2006; revised Oct. 24, 2006; accepted Oct. 24, 2006.
Correspondence should be addressed to Zoltan Nusser, Laboratory of Cellular Neurophysiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony Street 43, 1083 Budapest, Hungary. Email: nusser{at}koki.hu
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