Generation of resonance-dependent oscillation by mGluR-I activation switches single spiking to bursting in mesencephalic trigeminal sensory neurons

Gehoon Chung, Mitsuru Saito, Yasuhiro Kawasaki, Tsutomu Kawano, Dongxu Yin, Soojung Lee, Mikihiko Kogo, Masahiko Takada, Yong Chul Bae, Joong Soo Kim, Seog Bae Oh, Youngnam Kang

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

The primary sensory neurons supplying muscle spindles of jaw-closing muscles are unique in that they have their somata in the mesencephalic trigeminal nucleus (MTN) in the brainstem, thereby receiving various synaptic inputs. MTN neurons display bursting upon activation of glutamatergic synaptic inputs while they faithfully relay respective impulses arising from peripheral sensory organs. The persistent sodium current (INaP) is reported to be responsible for both the generation of bursts and the relay of impulses. We addressed how INaP is controlled either to trigger bursts or to relay respective impulses as single spikes in MTN neurons. Protein kinase C (PKC) activation enhanced INaP only at low voltages. Spike generation was facilitated by PKC activation at membrane potentials more depolarized than the resting potential. By injection of a ramp current pulse, a burst of spikes was triggered from a depolarized membrane potential whereas its instantaneous spike frequency remained almost constant despite the ramp increases in the current intensity beyond the threshold. A puff application of glutamate preceding the ramp pulse lowered the threshold for evoking bursts by ramp pulses while chelerythrine abolished such effects of glutamate. Dihydroxyphenylglycine, an agonist of mGluR1/5, also caused similar effects, and increased both the frequency and impedance of membrane resonance. Immunohistochemistry revealed that glutamatergic synapses are made onto the stem axons, and that mGluR1/5 and Nav1.6 are co-localized in the stem axon. Taken together, glutamatergic synaptic inputs onto the stem axon may be able to switch the relaying to the bursting mode.

Original languageEnglish
Pages (from-to)998-1012
Number of pages15
JournalEuropean Journal of Neuroscience
Volume41
Issue number8
DOIs
StatePublished - 1 Apr 2015

Keywords

  • Burst firing
  • Mesencephalic trigeminal nucleus
  • Metabotropic glutamate receptor
  • Persistent sodium current
  • Primary sensory neurons

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