Thermally active TRPV1 tonically drives central spontaneous glutamate release

Kiyomitsu Shoudai, James H. Peters, Stuart J. McDougall, Jessica A. Fawley, Michael Andresen

Research output: Contribution to journalArticle

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Abstract

Central synapses spontaneously release neurotransmitter at low rates. In the brainstem, cranial visceral afferent terminals in caudal solitary tract nucleus (NTS) display pronounced, activity-dependent, asynchronous release of glutamate and this extra release depends on TRPV1 receptors (TRPV1+). Asynchronous release is absent for afferents lacking TRPV1 (TRPV1-) and resting EPSC frequency was greater inTRPV1+. Here, we studied this basal activity difference by assessing thermal sensitivity of spontaneous and miniature synaptic events in TRPV1+ and TRPV1- second-order NTS neurons. The spontaneous EPSC rate decreased when temperature was decreased, increased steeply between 30 and 42° C only in TRPV1+ neurons, and was calcium-dependent. TRPV1-specific antagonist SB366791, but not TTX, strongly attenuated thermal responses. Temperature changes failed to alter EPSC frequency in TRPV1- neurons. EPSC amplitudes and decay kinetics changed little with temperature. IPSCs in these second-order NTS neurons were unaltered by temperature. Such results suggest that activated, presynaptic TRPV1+ receptors trigger continuous resting release of glutamate vesicles at physiological temperatures only in capsaicin-responsive terminals. In mechanically isolated individual neurons harvested from medial NTS, increases in temperature increased the rate of glutamate release only in TRPV1+ neurons, whereas IPSC rates were unaffected. Cadmium failed to block thermal increases in glutamate release, suggesting that calcium entry through TRPV1 channels may trigger glutamate release independently of voltage-activated calcium channels. Together, our findings indicate a new form of afferent signaling in which TRPV1 channels within central terminals of peripheral afferents tonically generate glutamate release in NTS at 37°C in the absence of afferent action potentials.

Original languageEnglish (US)
Pages (from-to)14470-14475
Number of pages6
JournalJournal of Neuroscience
Volume30
Issue number43
DOIs
StatePublished - Oct 27 2010

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Glutamic Acid
Neurons
Temperature
Hot Temperature
Visceral Afferents
Calcium
Presynaptic Receptors
Solitary Nucleus
Capsaicin
Calcium Channels
Cadmium
Synapses
Action Potentials
Brain Stem
Neurotransmitter Agents
TRPV1 receptor

ASJC Scopus subject areas

  • Neuroscience(all)

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Thermally active TRPV1 tonically drives central spontaneous glutamate release. / Shoudai, Kiyomitsu; Peters, James H.; McDougall, Stuart J.; Fawley, Jessica A.; Andresen, Michael.

In: Journal of Neuroscience, Vol. 30, No. 43, 27.10.2010, p. 14470-14475.

Research output: Contribution to journalArticle

Shoudai, Kiyomitsu ; Peters, James H. ; McDougall, Stuart J. ; Fawley, Jessica A. ; Andresen, Michael. / Thermally active TRPV1 tonically drives central spontaneous glutamate release. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 43. pp. 14470-14475.
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