Muscarinic M 4 receptors regulate GABAergic transmission in rat tuberomammillary nucleus neurons

Michiko Nakamura, Il Sung Jang

Research output: Contribution to journalArticlepeer-review

13 Scopus citations

Abstract

Histaminergic neurons within the tuberomammillary nucleus (TMN) play an important role in sleep-wakefulness regulation. Here, we report the muscarinic modulation of GABAergic spontaneous miniature inhibitory postsynaptic currents (mIPSCs) in mechanically dissociated rat histaminergic neurons using a conventional whole-cell patch clamp technique. Muscarine, a nonselective muscarinic acetylcholine (mACh) receptor agonist, reversibly decreased mIPSC frequency without affecting the current amplitude, indicating that muscarine acts presynaptically to decrease the probability of spontaneous GABA release. The muscarine action on GABAergic mIPSC frequency was completely blocked by atropine, a nonselective mACh receptor antagonist, and tropicamide, an M 4 receptor antagonist. The muscarine-induced decrease in mIPSC frequency was completely occluded in the presence of Cd 2+, a general voltage-dependent Ca 2+ channel blocker, or in a Ca 2+-free external solution. However, pharmacological agents affecting adenylyl cyclase or G-protein coupled inwardly rectifying K + channel activity did not prevent the inhibitory action of muscarine on GABAergic mIPSCs. These results suggest that muscarine acts on M 4 receptors on GABAergic nerve terminals projecting to histaminergic neurons to inhibit spontaneous GABA release via the inhibition of Ca 2+ influx from the extracellular space. Muscarine also inhibited action potential-dependent GABA release by activating presynaptic M 4 receptors in more physiological conditions. The M 4 receptor-mediated modulation of GABAergic transmission onto TMN neurons may contribute to the regulation of sleep-wakefulness. Highlights: Muscarine acted presynaptically to decrease GABAergic mIPSC frequency in TMN neurons. Tropicamide, an M 4 receptor antagonist, blocked the inhibitory action of muscarine on GABAergic mIPSCs. Muscarine decreased spontaneous GABA release by inhibiting Ca 2+ influx from the extracellular space. M 4 receptor activation decreased GABA release evoked by the electrical stimulation of the preoptic area.

Original languageEnglish
Pages (from-to)936-944
Number of pages9
JournalNeuropharmacology
Volume63
Issue number6
DOIs
StatePublished - Nov 2012

Keywords

  • MIPSCs
  • Patch clamp
  • Presynaptic M receptors
  • Sleep-wakefulness
  • Tuberomammillary nucleus

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