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The Journal of Neuroscience, May 19, 2004, 24(20):4709-4717; doi:10.1523/JNEUROSCI.0753-04.2004

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Cellular/Molecular
Purinergic and Vanilloid Receptor Activation Releases Glutamate from Separate Cranial Afferent Terminals in Nucleus Tractus Solitarius

Young-Ho Jin,¹ Timothy W. Bailey,¹ Bai-yan Li,² John H. Schild,² and Michael C. Andresen¹

¹Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239-3098, and ²Biomedical Engineering Program, Indiana University–Purdue University, Indianapolis, Indiana 46202-5132

Vanilloid (VR1) and purinergic (P2X) receptors are found in cranial afferent neurons in nodose ganglia and their central terminations within the solitary tract nucleus (NTS), but little is known about their function. We mechanically dissociated dorsomedial NTS neurons to preserve attached native synapses and tested for VR1 and P2X function primarily in spindle-shaped neurons resembling intact second-order neurons. All neurons (n = 95) exhibited spontaneous glutamate (EPSCs) and GABA (IPSCs)-mediated synaptic currents. VR1 agonist capsaicin (CAP; 100 nM) reversibly increased EPSC frequency, effects blocked by capsazepine. ATP (100 µM) increased EPSC frequency, actions blocked by P2X antagonist pyridoxalphosphate-6-azophenyl-2', 4'-disulfonic acid (PPADS; 20 µM). In all CAP-resistant neurons, P2X agonist -methylene-ATP (-m-ATP) increased EPSC frequency. Neither CAP nor -m-ATP altered EPSC amplitudes, kinetics, or holding currents. Thus, activation of VR1 and P2X receptors selectively facilitated presynaptic glutamate release on different NTS neurons. PPADS and 2',3'-O-(2,4,6-trinitrophenyl)-ATP blocked -m-ATP responses, but P2X1-selective antagonist NF023 (8,8'-[carbonylbis (imino-3,1-phenylene carbonylimino)]bis-1,3,5-naphthalenetrisulfonic acid) did not. The pharmacological profile and transient kinetics of ATP responses are consistent with P2X3 homomeric receptors. TTX and Cd²⁺ did not eliminate agonist-evoked EPSC frequency increases, suggesting that voltage-gated sodium and calcium channels are not required. In nodose ganglia, CAP but not -m-ATP evoked inward currents in slow conducting neurons and the converse pattern in myelinated, rapidly conducting neurons (n = 14). Together, results are consistent with segregation of glutamatergic terminals into either P2X sensitive or VR1 sensitive that correspondingly identify myelinated and unmyelinated afferent pathways at the NTS.

Key words: vanilloid; purinergic; presynaptic; glutamate; visceral afferent; brain stem

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Received Dec 15, 2003; revised April 5, 2004; accepted April 9, 2004.

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