Generation of resonance‐dependent oscillation by mGluR‐I activation switches single spiking to bursting in mesencephalic trigeminal sensory neurons. (25th February 2015)

• Record Type: Journal Article
• Authors: Chung, Gehoon; Saito, Mitsuru; Kawasaki, Yasuhiro; Kawano, Tsutomu; Yin, Dongxu; Lee, Soojung; Kogo, Mikihiko; Takada, Masahiko; Bae, Yong Chul; Kim, Joong Soo; Oh, Seog Bae; Kang, Youngnam
• Is Part Of: European journal of neuroscience. Volume 41:Number 8(2015:Apr.)
• Page Start: 998
• Page End: 1012
• Publication Date: 2015-02-25
• Subjects: burst firing -- mesencephalic trigeminal nucleus -- metabotropic glutamate receptor -- persistent sodium current -- primary sensory neurons; Nervous system -- Periodicals; 612.8
• DOI: 10.1111/ejn.12858
• Languages: English
• ISSNs: 0953-816X

Abstract

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 ( I N aP ) is reported to be responsible for both the generation of bursts and the relay of impulses. We addressed how I N aP is controlled either to trigger bursts or to relay respective impulses as single spikes in MTN neurons. Protein kinase C (PKC) activation enhanced I N aP 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. Abstract : Glutamatergic synapses were made onto the stem axon of the primary sensory neuron in the mesencephalic trigeminal nucleus (MTN). Glutamatergic synaptic action upregulates I NaP by activation of PKC in the stem axon where mGluR1/5 and Nav1.6 were co‐localized, to trigger bursts. The strategic location of glutamatergic synapses on the stem axon plays a crucial role in switching the firing mode of MTN neurons from the relay mode as primary sensory neurons to the bursting one as premotor neurons.