Opposite roles in short-term plasticity for N-type and P/Q-type voltage-dependent calcium channels in gabaergic neuronal connections in the rat cerebral cortex

Kiyofumi Yamamoto, Masayuki Kobayashi

Research output: Contribution to journalArticlepeer-review

22 Citations (Scopus)

Abstract

Neurotransmitter release is triggered by Ca2+ influx through voltage-dependent Ca2+ channels (VDCCs). Distinct expression patterns of VDCC subtypes localized on the synaptic terminal affect intracellular Ca2+ dynamics induced by action potential-triggered Ca2+ influx. However, it has been unknown whether the expression pattern of VDCC subtypes depends on each axon terminal or neuronal subtype. Furthermore, little information is available on how these VDCC subtypes regulate the release probability of neurotransmitters. To address these questions, we performed multiple whole-cell patch-clamp recordings from GABAergic neurons in the insular cortex of either the male or the female rat. The paired-pulse ratio (PPR; 50 ms interstimulus interval) varied widely among inhibitory connections between GABAergic neurons. The PPR of unitary IPSCs was enhanced by ω-conotoxin GVIA (CgTx; 3 μM), an N-type VDCC blocker, whereas blockade of P/Q-type VDCCs by ω-agatoxin IVA (AgTx, 200 nM) decreased the PPR. In the presence of CgTx, application of 4 mM [Ca2+]o or of roscovitine, a P/Q-type activator, increased the PPR. These results suggest that the recruitment of P/Q-type VDCCs increases the PPR, whereas N-type VDCCs suppress the PPR. Furthermore, we found that charybdotoxin or apamin, blockers of Ca2+-dependent K+ channels, with AgTx increased the PPR, suggesting that Ca2+-dependent K+ channels are coupled to N-type VDCCs and suppress the PPR in GABAergic neuronal terminals. Variance–mean analysis with changing [Ca2+]o showed a negative correlation between the PPR and release probability in GABAergic synapses. These results suggest that GABAergic neurons differentially express N-type and/or P/Q-type VDCCs and that these VDCCs regulate the GABA release probability in distinct manners.

Original languageEnglish
Pages (from-to)9814-9828
Number of pages15
JournalJournal of Neuroscience
Volume38
Issue number46
DOIs
Publication statusPublished - 14 Nov 2018

Keywords

  • Agranular
  • AI
  • Calcium channel
  • Parvalbumin
  • STP
  • VGCC

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