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The Journal of Neuroscience, November 1, 2002, 22(21):9237-9243

Kainate Receptor-Dependent Short-Term Plasticity of Presynaptic Ca²⁺ Influx at the Hippocampal Mossy Fiber Synapses

Haruyuki Kamiya^{1, 2}, Seiji Ozawa^{2, 3}, and Toshiya Manabe^{1, 4}

¹ Division of Cell Biology and Neurophysiology, Department of Neuroscience, Faculty of Medicine, Kobe University, Kobe, Hyogo 650-0017, Japan, ² Department of Physiology, Gunma University School of Medicine, Maebashi, Gunma 371-8511, Japan, ³ Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Kawaguchi, Saitama 332-0012, Japan, and ⁴ Division of Neuronal Network, Department of Basic Medical Sciences, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan

Transmitter release at the hippocampal mossy fiber (MF)-CA3 synapse exhibits robust use-dependent short-term plasticity with an extremely wide dynamic range. Recent studies revealed that presynaptic kainate receptors (KARs), which specifically localized on the MF axons, mediate unusually large facilitation at this particular synapse in concert with the action of residual Ca²⁺. However, it is currently unclear how activation of kainate autoreceptors enhances transmitter release in an activity-dependent manner. Using fluorescence recordings of presynaptic Ca²⁺ and voltage in hippocampal slices, here we demonstrate that paired-pulse stimulation (with 20-200 msec intervals) resulted in facilitation of Ca²⁺ influx into the MF terminals, as opposed to other synapses, such as the Schaffer collateral-CA1 synapse. These observations deviate from typical residual Ca²⁺ hypothesis of facilitation, assuming an equal amount of Ca²⁺ influx per action potential. Pharmacological experiments reveal that the facilitation of presynaptic Ca²⁺ influx is mediated by activation of KARs. We also found that action potentials of MF axons are followed by prominent afterdepolarization, which is partly mediated by activation of KARs. Notably, the time course of the afterdepolarization approximates to that of the paired-pulse facilitation of Ca²⁺ influx, suggesting that these two processes are closely related to each other. These results suggest that the novel mechanism amplifying presynaptic Ca²⁺ influx may underlie the robust short-term synaptic plasticity at the MF-CA3 synapse in the hippocampus, and this process is mediated by KARs whose activation evokes prominent afterdepolarization of MF axons and thereby enhances action potential-driven Ca²⁺ influx into the presynaptic terminals.

Key words: hippocampus; kainate receptor; mossy fiber; paired-pulse facilitation; presynaptic Ca²⁺ influx; short-term plasticity

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22219237-07$05.00/0

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