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The Journal of Neuroscience, January 24, 2007, 27(4):942-950; doi:10.1523/JNEUROSCI.4996-06.2007

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Cellular/Molecular
GABAergic Spill-Over Transmission onto Hippocampal Mossy Fiber Boutons

Henrik Alle and Jörg R. P. Geiger

Independent Hertie Research Group, Max Planck Institute for Brain Research, D-60528 Frankfurt, Germany

Correspondence should be addressed to Jörg R. P. Geiger, Independent Hertie Research Group, Max Planck Institute for Brain Research, Deutschordenstrasse 46, D-60528 Frankfurt, Germany. Email: geiger{at}mpih-frankfurt.mpg.de

Presynaptic ionotropic GABA_A receptors have been suggested to contribute to the regulation of cortical glutamatergic synaptic transmission. Here, we analyzed presynaptic GABA_A receptor-mediated currents (34°C) recorded from mossy fiber boutons (MFBs) in rat hippocampal slices. In MFBs from young and adult animals, GABA puff application activated currents that were blocked by GABA_A receptor antagonists. The conductance density of 0.65 mS · cm² was comparable to that of other presynaptic terminals. The single-channel conductance was 36 pS (symmetrical chloride), yielding an estimated GABA_A receptor density of 20–200 receptors per MFB. Presynaptic GABA_A receptors likely contain ₂-subunits as indicated by their zolpidem sensitivity. In accordance with the low apparent GABA affinity (EC₅₀ = 60 µM) of the receptors and a tight control of ambient GABA concentration by GABA transporters, no tonic background activation of presynaptic GABA_A receptors was observed. Instead, extracellular high-frequency stimulation led to transient presynaptic currents, which were blocked by GABA_A receptor antagonists but were enhanced by block of GAT 1 (GABA transporter 1), indicating that these currents were generated by GABA spill-over and subsequent presynaptic GABA_A receptor activation. Presynaptic spill-over currents were depressed by pharmacological cannabinoid 1 (CB1) receptor activation, suggesting that GABA was released predominantly by a CB1 receptor-expressing interneuron subpopulation. Because GABA_A receptors in axons are considered to act depolarizing, high activity of CB1 receptor-expressing interneurons will exert substantial impact on presynaptic membrane potential, thus modulating action potential-evoked transmitter release at the mossy fiber–CA3 synapse.

Key words: hippocampal mossy fiber; presynaptic; GABA_A receptor; spill-over; zolpidem; GAT

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Received Nov. 17, 2006; revised Dec. 18, 2006; accepted Dec. 19, 2006.

Correspondence should be addressed to Jörg R. P. Geiger, Independent Hertie Research Group, Max Planck Institute for Brain Research, Deutschordenstrasse 46, D-60528 Frankfurt, Germany. Email: geiger{at}mpih-frankfurt.mpg.de

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