Ca2+-activated ion currents triggered by ryanodine receptor-mediated Ca2+release control firing of inhibitory neurons in the prepositus hypoglossi nucleus

Author:

Saito Yasuhiko1,Yanagawa Yuchio12

Affiliation:

1. Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan; and

2. Japan Science and Technology Agency, Core Research for Evolutional Science and Technology (CREST), Sanbancho, Chiyoda-ku, Tokyo, Japan

Abstract

Spontaneous miniature outward currents (SMOCs) are known to exist in smooth muscles and peripheral neurons, and evidence for the presence of SMOCs in central neurons has been accumulating. SMOCs in central neurons are induced through Ca2+-activated K+(KCa) channels, which are activated through Ca2+-induced Ca2+release from the endoplasmic reticulum via ryanodine receptors (RyRs). Previously, we found that some neurons in the prepositus hypoglossi nucleus (PHN) showed spontaneous outward currents (SOCs). In the present study, we used whole cell recordings in slice preparations of the rat brain stem to investigate the following: 1) the ionic mechanisms of SOCs, 2) the types of neurons exhibiting frequent SOCs, and 3) the effect of Ca2+-activated conductance on neuronal firing. Pharmacological analyses revealed that SOCs were induced via the activation of small-conductance-type KCa(SK) channels and RyRs, indicating that SOCs correspond to SMOCs. An analysis of the voltage responses to current pulses of the fluorescence-expressing inhibitory neurons of transgenic rats revealed that inhibitory neurons frequently exhibited SOCs. Abolition of SOCs via blockade of SK channels enhanced the frequency of spontaneous firing of inhibitory PHN neurons. However, abolition of SOCs via blockade of RyRs reduced the firing frequency and hyperpolarized the membrane potential. Similar reductions in firing frequency and hyperpolarization were also observed when Ca2+-activated nonselective cation (CAN) channels were blocked. These results suggest that, in inhibitory neurons in the PHN, Ca2+release via RyRs activates SK and CAN channels, and these channels regulate spontaneous firing in a complementary manner.

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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