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J Neurophysiol 97: 503-511, 2007. First published October 25, 2006; doi:10.1152/jn.01023.2006
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TRPV1 Receptor Mediates Glutamatergic Synaptic Input to Dorsolateral Periaqueductal Gray (dl-PAG) Neurons

Jihong Xing and Jianhua Li

Heart and Vascular Institute and Department of Medicine, The Pennsylvania State University College of Medicine, Milton S. Hershey Medical Center, Hershey, Pennsylvania

Submitted 26 September 2006; accepted in final form 24 October 2006

The purpose of this study was to determine the role of transient receptor potential vanilloid type 1 (TRPV1) receptor in modulating neuronal activity of the dorsolateral periaqueductal gray (dl-PAG) through excitatory and inhibitory synaptic inputs. First, whole cell voltage-clamp recording was performed to obtain the spontaneous miniature excitatory postsynaptic currents (mEPSCs) and inhibitory postsynaptic currents (mIPSCs) of the dl-PAG neurons. As 1 µM of capsaicin was applied into the perfusion chamber, the frequency of mEPSCs was increased from 3.21 ± 0.49 to 5.64 ± 0.64 Hz (P < 0.05, n = 12) without altering the amplitude and the decay time constant of mEPSCs. In contrast, capsaicin had no distinct effect on mIPSCs. A specific TRPV1 receptor antagonist, iodo-resiniferatoxin (i-RTX, 300 nM), decreased the frequency of mEPSCs from 3.51 ± 0.29 to 2.01 ± 0.2 Hz (P < 0.05, n = 8) but did not alter the amplitude and decay time. In addition, i-RTX applied into the chamber abolished the effect of capsaicin on mEPSC of the dl-PAG. In another experiment, spontaneous action potential of the dl-PAG neurons was recorded using whole cell current-clamp methods. Capsaicin significantly elevated the discharge rate of the dl-PAG neurons from 3.03 ± 0.38 to 5.96 ± 0.87 Hz (n = 8). The increased firing activity was abolished in the presence of glutamate N-methy-D-aspartate (NMDA) and non-NMDA antagonists, 2-amino-5-phosphonopentanoic acid, and 6-cyano-7-nitroquinoxaline-2,3-dione. The results from this study provide the first evidence indicating that activation of TRPV1 receptors increases the neuronal activity of the dl-PAG through selective potentiation of glutamatergic synaptic inputs.


Address for reprint requests and other correspondence: J. Li, Heart and Vascular Inst. and Div. of Cardiology, H047, Pennsylvania State Univ. College of Medicine, Milton S. Hershey Medical Ctr., 500 University Dr., Hershey, PA 17033 (E-mail: jzl10{at}psu.edu)




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