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Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse

Haruyuki Kamiya and Seiji Ozawa

1. The presynaptic action of kainate (KA) receptor activation at the mossy fibre-CA3 synapse was examined using fluorescence measurement of presynaptic Ca²⁺ influx as well as electrophysiological recordings in mouse hippocampal slices.

2. Bath application of a low concentration (0·2 µM) of KA reversibly increased the amplitude of presynaptic volley evoked by stimulation of mossy fibres to 146 ± 6 % of control (n = 6), whereas it reduced the field excitatory postsynaptic potential (EPSPs) to 30 ± 4 %.

3. The potentiating effect of KA on the presynaptic volleys was also observed in Ca²⁺-free solution, and was partly antagonized by (2S,4R)-4-methylglutamic acid (SYM 2081, 1 µM), which selectively desensitizes KA receptors.

4. The antidromic population spike of dentate granule cells evoked by stimulation of mossy fibres was increased by application of 0·2 µM KA to 160 ± 10 % of control (n = 6). Whole-cell current-clamp recordings revealed that the stimulus threshold for generating antidromic spikes recorded from a single granule cell was lowered by KA application.

5. Application of KA (0·2 µM) suppressed presynaptic Ca²⁺ influx to 78 ± 4 % of control (n = 6), whereas the amplitude of the presynaptic volley was increased.

6. KA at 0·2 µM reversibly suppressed excitatory postsynaptic currents (EPSCs) evoked by mossy fibre simulation to 38 ± 9 % of control (n = 5).

7. These results suggest that KA receptor activation enhances the excitability of mossy fibres, probably via axonal depolarization, and reduces action potential-induced Ca²⁺ influx, thereby inhibiting mossy fibre EPSCs presynaptically. This novel presynaptic inhibitory action of KA at the mossy fibre-CA3 synapse may regulate the excitability of highly interconnected CA3 networks.

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