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J Neurophysiol 88: 2664-2674, 2002; doi:10.1152/jn.00540.2002
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J Neurophysiol (November 1, 2002). 10.1152/jn.00540.2002
Submitted on 24 July 2002
Accepted on 1 August 2002

Nitric Oxide Inhibits Spinally Projecting Paraventricular Neurons Through Potentiation of Presynaptic GABA Release

De-Pei Li,1 Shao-Rui Chen,1 and Hui-Lin Pan1,2

 1Department of Anesthesiology and  2Department of Neuroscience and Anatomy, The Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033

Li, De-Pei, Shao-Rui Chen, and Hui-Lin Pan. Nitric Oxide Inhibits Spinally Projecting Paraventricular Neurons Through Potentiation of Presynaptic GABA Release. J. Neurophysiol. 88: 2664-2674, 2002. Nitric oxide (NO) in the paraventricular nucleus (PVN) is involved in the regulation of the excitability of PVN neurons. However, the effect of NO on the inhibitory GABAergic and excitatory glutamatergic inputs to spinally projecting PVN neurons has not been studied specifically. In the present study, we determined the role of the inhibitory GABAergic and excitatory glutamatergic inputs in the inhibitory action of NO on spinally projecting PVN neurons. Spinally projecting PVN neurons were retrogradely labeled by a fluorescent dye, 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocasbocyane (DiI), injected into the spinal cord of rats. Whole cell voltage- and current-clamp recordings were performed on DiI-labeled PVN neurons in the hypothalamic slice. The spontaneous miniature inhibitory postsynaptic currents (mIPSCs) recorded in DiI-labeled neurons were abolished by 20 µM bicuculline, whereas the miniature excitatory postsynaptic currents (mEPSCs) were eliminated by 20 µM 6-cyano-7-nitroquinoxaline-2,3-dione. Bath application of an NO donor, 100 µM S-nitroso-N-acetyl-penicillamine (SNAP), or the NO precursor, 100 µM L-arginine, both significantly increased the frequency of mIPSCs of DiI-labeled PVN neurons, without altering the amplitude and the decay time constant of mIPSCs. The effect of SNAP and L-arginine on the frequency of mIPSCs was eliminated by an NO scavenger, 2-(4-carboxypheny)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide, and an NO synthase inhibitor, 1-(2-trifluoromethylphenyl) imidazole, respectively. Neither SNAP nor L-arginine significantly altered the frequency and the amplitude of mEPSCs. Under current-clamp conditions, 100 µM SNAP or 100 µM L-arginine significantly decreased the discharge rate of the DiI-labeled PVN neurons, without significantly affecting the resting membrane potential. On the other hand, 20 µM bicuculline significantly increased the impulse activity of PVN neurons. In the presence of bicuculline, SNAP or L-arginine both failed to inhibit the firing activity of PVN neurons. This electrophysiological study provides substantial new evidence that NO suppresses the activity of spinally projecting PVN neurons through potentiation of the GABAergic synaptic input.




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