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Presynaptic 5-HT₃ receptor-mediated modulation of synaptic GABA release in the mechanically dissociated rat amygdala neurons

Susumu Koyama *†, Nozomu Matsumoto *, Chiharu Kubo † and Norio Akaike *

1. Nystatin-perforated patch recordings were made from mechanically dissociated basolateral amygdala neurons with preserved intact native presynaptic nerve terminals to study the mechanism of 5-HT₃ receptor-mediated serotonergic modulation of GABAergic inhibition.

2. The specific 5-HT₃ agonist mCPBG (1 µM) rapidly facilitated the frequency of GABAergic miniature inhibitory postsynaptic currents (mIPSCs) and this facilitation desensitized within 1 min. Tropisetron (30 nM), a specific 5-HT₃ antagonist, blocked the mCPBG effect.

3. mCPBG augmented mIPSC amplitude. However, no direct postsynaptic serotonergic currents were evoked by mCPBG. Neither GABA-evoked current amplitude nor the kinetics of individual GABAergic mIPSCs were affected by mCPBG. Therefore, the augmentation is unlikely to be due to postsynaptic effects evoked by mCPBG. At higher concentrations mCPBG produced shorter-duration facilitation of miniature events.

4. While mCPBG increased the mIPSC frequency in calcium-containing solution with Cd²⁺, this increase was absent in Ca²⁺-free external solution. It appears that the Ca²⁺ influx through voltage-dependent calcium channels was not as crucial as that through 5-HT₃ receptors for synaptic GABA release.

5. When two pulses of mCPBG (each 1 µM, 1 min) were given, the response to the second pulse elicited full recovery when the interval between pulses was at least 9 min. Protein kinase A (PKA) activation by 8-Br-cAMP (300 µM) shortened and PKA inhibition by Rp-cAMP (100 µM) prolonged the recovery time. PKA activity did not affect the time course of fast desensitization.

6. Our results suggest that a 5-HT₃-specific agonist acts on presynaptic nerve terminals facilitating synaptic GABA release without postsynaptic effects. The facilitation requires calcium influx through presynaptic 5-HT₃ receptors. PKA modulates the recovery process from desensitization of presynaptic 5-HT₃ receptor-mediated regulation of synaptic GABA release.

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