Arizona Health Sciences

Physiological temperatures drive glutamate release onto trigeminal superficial dorsal horn neurons.

TitlePhysiological temperatures drive glutamate release onto trigeminal superficial dorsal horn neurons.
Publication TypeJournal Article
Year of Publication2014
AuthorsLargent-Milnes TM, Hegarty DM, Aicher SA, Andresen MC
JournalJ Neurophysiol
Volume111
Issue11
Pagination2222-31
Date Published2014 Jun 01
ISSN1522-1598
KeywordsAnimals, Body Temperature Regulation, Glutamic Acid, Ion Channel Gating, Male, Neurotransmitter Agents, Posterior Horn Cells, Rats, Rats, Sprague-Dawley, Synaptic Transmission, Thermosensing, Trigeminal Nuclei, TRPV Cation Channels
Abstract

Trigeminal sensory afferent fibers terminating in nucleus caudalis (Vc) relay sensory information from craniofacial regions to the brain and are known to express transient receptor potential (TRP) ion channels. TRP channels are activated by H(+), thermal, and chemical stimuli. The present study investigated the relationships among the spontaneous release of glutamate, temperature, and TRPV1 localization at synapses in the Vc. Spontaneous excitatory postsynaptic currents (sEPSCs) were recorded from Vc neurons (n = 151) in horizontal brain-stem slices obtained from Sprague-Dawley rats. Neurons had basal sEPSC rates that fell into two distinct frequency categories: High (≥10 Hz) or Low (<10 Hz) at 35°C. Of all recorded neurons, those with High basal release rates (67%) at near-physiological temperatures greatly reduced their sEPSC rate when cooled to 30°C without amplitude changes. Such responses persisted during blockade of action potentials indicating that the High rate of glutamate release arises from presynaptic thermal mechanisms. Neurons with Low basal frequencies (33%) showed minor thermal changes in sEPSC rate that were abolished after addition of TTX, suggesting these responses were indirect and required local circuits. Activation of TRPV1 with capsaicin (100 nM) increased miniature EPSC (mEPSC) frequency in 70% of neurons, but half of these neurons had Low basal mEPSC rates and no temperature sensitivity. Our evidence indicates that normal temperatures (35-37°C) drive spontaneous excitatory synaptic activity within superficial Vc by a mechanism independent of presynaptic action potentials. Thus thermally sensitive inputs on superficial Vc neurons may tonically activate these neurons without afferent stimulation.

DOI10.1152/jn.00912.2013
Alternate JournalJ. Neurophysiol.
PubMed ID24598529
PubMed Central IDPMC4097869
Grant ListF32 DE022499 / DE / NIDCR NIH HHS / United States
DE-12640 / DE / NIDCR NIH HHS / United States
HL-105703 / HL / NHLBI NIH HHS / United States
R01 HL105703 / HL / NHLBI NIH HHS / United States
F32-DE-022499 / DE / NIDCR NIH HHS / United States
Faculty Member Reference: 
Tally Largent-Milnes, Ph.D.