Journal article
Thermally Active TRPV1 Tonically Drives Central Spontaneous Glutamate Release
The Journal of neuroscience, Vol.30(43), pp.14470-14475
10/27/2010
Handle:
https://hdl.handle.net/2376/109958
PMCID: PMC2976575
PMID: 20980604
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 in TRPV1+. 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.
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Details
- Title
- Thermally Active TRPV1 Tonically Drives Central Spontaneous Glutamate Release
- Creators
- Kiyomitsu Shoudai - Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239James H Peters - Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239Stuart J McDougall - Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239Jessica A Fawley - Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239Michael C Andresen - Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239
- Publication Details
- The Journal of neuroscience, Vol.30(43), pp.14470-14475
- Academic Unit
- Integrative Physiology and Neuroscience, Department of
- Publisher
- Society for Neuroscience
- Identifiers
- 99900547493001842
- Language
- English
- Resource Type
- Journal article