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The Journal of Neuroscience, February 7, 2007, 27(6):1365-1373; doi:10.1523/JNEUROSCI.4672-06.2007

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Cellular/Molecular
GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus

Michiko Nakamura,¹ Yuko Sekino,^1,2 and Toshiya Manabe^1,2

¹Division of Neuronal Network, Department of Basic Medical Sciences, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan, and ²Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Kawaguchi, 332-0012, Japan

Correspondence should be addressed to Toshiya Manabe, Division of Neuronal Network, Department of Basic Medical Sciences, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan. Email: tmanabe-tky{at}umin.ac.jp

Profound activity-dependent synaptic facilitation at hippocampal mossy fiber synapses is a unique and functionally important property. Although presynaptic ionotropic receptors, such as kainate receptors, contribute partially to the facilitation in the hippocampus, the precise mechanisms of presynaptic regulation by endogenous neurotransmitters remain unclear. In this study, we report that axonal GABA_A receptors on mossy fibers are involved in the activity-dependent facilitation during development. In immature mouse hippocampal slices, short-train stimulation (five pulses at 25 Hz) caused frequency-dependent facilitation of not only postsynaptic responses but also presynaptic fiber volleys that represent presynaptic activities. This fiber volley facilitation was inhibited by selective GABA_A receptor antagonists, or by enkephalin that selectively suppresses excitability of interneurons. Furthermore, we directly demonstrated that this facilitation resulted from depolarization of mossy fibers in imaging experiments using a voltage-sensitive dye. This increased mossy fiber excitability caused by depolarizing action of GABA gradually decreased with development and eventually disappeared at around postnatal day 30. These results suggested that GABA released from interneurons acted on axonal GABA_A receptors on mossy fibers and contributed at least partially to the activity- and age-dependent facilitation in the hippocampus.

Key words: GABA_A receptor; hippocampus; synaptic transmission; development; mossy fiber; presynaptic facilitation

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Received Aug. 10, 2006; revised Dec. 25, 2006; accepted Dec. 29, 2006.

Correspondence should be addressed to Toshiya Manabe, Division of Neuronal Network, Department of Basic Medical Sciences, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan. Email: tmanabe-tky{at}umin.ac.jp

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