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J Neurophysiol (April 28, 2004). doi:10.1152/jn.00171.2004
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Submitted on February 23, 2004
Accepted on April 24, 2004

VR1 Receptor Activation Induces Glutamate Release and Postsynaptic Firing in the Paraventricular Nucleus

De-Pei Li, Shao-Rui Chen, and Hui-Lin Pan*

* To whom correspondence should be addressed. E-mail: hpan{at}psu.edu.

Neurons in the paraventricular nucleus (PVN) are important in regulating autonomic function through projections to the brainstem and spinal cord. Although the vanilloid receptors (VR1) are present in the PVN, their physiological function is little known. In this study, we determined the role of VR1 receptors in the regulation of synaptic inputs and the excitability of spinally projecting PVN neurons. Whole-cell patch-clamp recordings were performed on the PVN neurons labeled by a retrograde fluorescence tracer injected into the thoracic spinal cord of rats. Capsaicin significantly increased the frequency of glutamatergic mEPSCs without changing the amplitude and decay time constant of mEPSCs. On the other hand, capsaicin had no effect on GABAergic mIPSCs. The effect of capsaicin on mEPSCs was abolished by a specific VR1 antagonist, iodo-resiniferatoxin, or ruthenium red. Importantly, iodo-resiniferatoxin per se significantly reduced the amplitude of evoked EPSCs and the frequency of mEPSCs. Removal of extracellular Ca2+, but not Cd2+ treatment, also eliminated the effect of capsaicin on mEPSCs. Furthermore, capsaicin caused a large increase in the firing rate of PVN neurons, and such an effect was abolished in the presence of ionotropic glutamate receptor antagonists. Additionally, the double immunofluorescence labeling revealed that all of the VR1 immunoreactivity was colocalized with a presynaptic marker, synaptophysin, in the PVN. Thus, this study provides the first evidence that activation of VR1 receptors excites pre-autonomic PVN neurons through selective potentiation of glutamatergic synaptic inputs. Presynaptic VR1 receptors and endogenous capsaicin-like substances in the PVN may represent a previously unidentified mechanism in hypothalamic regulation of the autonomic nervous system.




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