Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents.
Temperature is fundamentally important to all biological functions including synaptic glutamate release. Vagal afferents from the solitary tract (ST) synapse on second order neurons in the nucleus of the solitary tract, and glutamate release at this first central synapse controls autonomic reflex fu...
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doaj-3446fca003624d65b48c15b78ecf18df2020-11-25T01:31:38ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01105e012776410.1371/journal.pone.0127764Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents.Jessica A FawleyMackenzie E HofmannTally M Largent-MilnesMichael C AndresenTemperature is fundamentally important to all biological functions including synaptic glutamate release. Vagal afferents from the solitary tract (ST) synapse on second order neurons in the nucleus of the solitary tract, and glutamate release at this first central synapse controls autonomic reflex function. Expression of the temperature-sensitive Transient Receptor Potential Vanilloid Type 1 receptor separates ST afferents into C-fibers (TRPV1+) and A-fibers (TRPV1-). Action potential-evoked glutamate release is similar between C- and A-fiber afferents, but TRPV1 expression facilitates a second form of synaptic glutamate release in C-fibers by promoting substantially more spontaneous glutamate release. The influence of temperature on different forms of glutamate release is not well understood. Here we tested how temperature impacts the generation of evoked and spontaneous release of glutamate and its relation to TRPV1 expression. In horizontal brainstem slices of rats, activation of ST primary afferents generated synchronous evoked glutamate release (ST-eEPSCs) at constant latency whose amplitude reflects the probability of evoked glutamate release. The frequency of spontaneous EPSCs in these same neurons measured the probability of spontaneous glutamate release. We measured both forms of glutamate from each neuron during ramp changes in bath temperature of 4-5 °C. Spontaneous glutamate release from TRPV1+ closely tracked with these thermal changes indicating changes in the probability of spontaneous glutamate release. In the same neurons, temperature changed axon conduction registered as latency shifts but ST-eEPSC amplitudes were constant and independent of TRPV1 expression. These data indicate that TRPV1-operated glutamate release is independent of action potential-evoked glutamate release in the same neurons. Together, these support the hypothesis that evoked and spontaneous glutamate release originate from two pools of vesicles that are independently modulated and are distinct processes.http://europepmc.org/articles/PMC4439140?pdf=render |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Jessica A Fawley Mackenzie E Hofmann Tally M Largent-Milnes Michael C Andresen |
spellingShingle |
Jessica A Fawley Mackenzie E Hofmann Tally M Largent-Milnes Michael C Andresen Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents. PLoS ONE |
author_facet |
Jessica A Fawley Mackenzie E Hofmann Tally M Largent-Milnes Michael C Andresen |
author_sort |
Jessica A Fawley |
title |
Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents. |
title_short |
Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents. |
title_full |
Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents. |
title_fullStr |
Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents. |
title_full_unstemmed |
Temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents. |
title_sort |
temperature differentially facilitates spontaneous but not evoked glutamate release from cranial visceral primary afferents. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS ONE |
issn |
1932-6203 |
publishDate |
2015-01-01 |
description |
Temperature is fundamentally important to all biological functions including synaptic glutamate release. Vagal afferents from the solitary tract (ST) synapse on second order neurons in the nucleus of the solitary tract, and glutamate release at this first central synapse controls autonomic reflex function. Expression of the temperature-sensitive Transient Receptor Potential Vanilloid Type 1 receptor separates ST afferents into C-fibers (TRPV1+) and A-fibers (TRPV1-). Action potential-evoked glutamate release is similar between C- and A-fiber afferents, but TRPV1 expression facilitates a second form of synaptic glutamate release in C-fibers by promoting substantially more spontaneous glutamate release. The influence of temperature on different forms of glutamate release is not well understood. Here we tested how temperature impacts the generation of evoked and spontaneous release of glutamate and its relation to TRPV1 expression. In horizontal brainstem slices of rats, activation of ST primary afferents generated synchronous evoked glutamate release (ST-eEPSCs) at constant latency whose amplitude reflects the probability of evoked glutamate release. The frequency of spontaneous EPSCs in these same neurons measured the probability of spontaneous glutamate release. We measured both forms of glutamate from each neuron during ramp changes in bath temperature of 4-5 °C. Spontaneous glutamate release from TRPV1+ closely tracked with these thermal changes indicating changes in the probability of spontaneous glutamate release. In the same neurons, temperature changed axon conduction registered as latency shifts but ST-eEPSC amplitudes were constant and independent of TRPV1 expression. These data indicate that TRPV1-operated glutamate release is independent of action potential-evoked glutamate release in the same neurons. Together, these support the hypothesis that evoked and spontaneous glutamate release originate from two pools of vesicles that are independently modulated and are distinct processes. |
url |
http://europepmc.org/articles/PMC4439140?pdf=render |
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