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J Neurophysiol (April 19, 2006). doi:10.1152/jn.00176.2006
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Submitted on February 17, 2006
Accepted on April 14, 2006

Two Opposing Roles of 4-AP-sensitive K+ Current in Initiation and Invasion of Spikes in Rat Mesencephalic Trigeminal Neurons

Mitsuru Saito1, Yoshinaka Murai2, Hajime Sato1, Yong-Chul Bae3, Tadashi Akaike4, Masahiko Takada5, and Youngnam Kang6*

1 Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka, Japan
2 Department of Physiology, , School of Medicine, Kurume University, Kurume, Japan
3 Department of Oral Anatomy, School of Dentistry, Kyungpook National University, Daegu, Korea, Republic of
4 Department of Oral Functional Science (Physiology), Graduate School of Dental Medicine, Hokkaido University, Sapporo, Japan
5 Department of System Neuroscience, Tokyo Metropolitan Institute for Neuroscience, Tokyo Metropolitan Organization for Medical Research, Fuchu, Tokyo, Japan
6 Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka, Japan; Health Sciences University of Hokkaido, Research Institute of Personalized Health Sciences, Ishikari-Tobetsu, Hokkaido, Japan

* To whom correspondence should be addressed. E-mail: kang{at}dent.osaka-u.ac.jp.

The axon initial segment plays important roles in spike initiation and invasion of axonal-spikes into the soma. Among primary sensory neurons, those in the mesencephalic trigeminal nucleus (MTN) are exceptional in their ability to initiate soma-spikes (S-spikes) in response to synaptic inputs, consequently displaying two kinds of S-spikes, one caused by invasion of an axonal-spike arising from the sensory receptor and the other initiated by somatic inputs. We investigated where spikes are initiated in such MTN neurons and whether there are any differences between the two kinds of S-spikes. Simultaneous patch-clamp recordings from the soma and axon hillock revealed a spike-backpropagation from the spike-initiation site in the stem axon to the soma in response to 1-ms somatic current pulse, which disclosed the delayed emergence of S-spikes after the current pulse offset. These initiated S-spikes were smaller in amplitude than S-spikes generated by stimulation of the stem axon; however, 4-AP (≤0.5mM) eliminated the amplitude difference. Furthermore, 4-AP markedly shortened the delay in spike initiation without affecting the spike-backpropagation time in the stem axon, whereas it markedly prolonged the refractory period of S-spikes arising from axonal-spike-invasion without markedly affecting that of presumed axonal-spikes. These observations suggest that 4-AP-sensitive K+ currents exert two opposing effects on S-spikes depending on their origins; suppression of spike initiation and facilitation of axonal-spike-invasion at higher frequencies. Consistent with these findings, strong immunoreactivities for Kv1.1 and Kv1.6, among 4-AP-sensitive and low-voltage-activated Kv1 family examined, were detected in the soma but not in the stem axon of MTN neurons.




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