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- Title
Thermally Active TRPV1 Tonically Drives Central Spontaneous Glutamate Release.
- Authors
Shoudai, Kiyomitsu; Peters, James H.; McDougall, Stuart J.; Fawley, Jessica A.; Andresen, Michael C.
- 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 TRPV 1 (TRPV1 -) and resting EPSC frequency was greater in TRPV 1+. 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. TRPVI-specifIc antagonist SB366791, but not lix, strongly attenuated thermal responses. Temperature changes failed to alter EPSC frequency in TRPV1 - neurons. EPSC ampli- tudes 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.
- Subjects
SOLITARY nucleus; NEURAL transmission; SOMATOSENSORY evoked potentials; NEUROTRANSMITTERS; NEURONS; BRAIN stem physiology; AFFERENT pathways; PHYSIOLOGY
- Publication
Journal of Neuroscience, 2010, Vol 30, Issue 43, p14470
- ISSN
0270-6474
- Publication type
Article
- DOI
10.1523/JNEUROSCI.2557-10.2010