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The Journal of Neuroscience, March 1, 2003, 23(5):1941
On the Role of Nitric Oxide in Hippocampal Long-Term Potentiation
Christelle L. M. Bon and John Garthwaite The Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, United Kingdom
Nitric oxide (NO) functions in several types of synaptic plasticity, including hippocampal long-term potentiation (LTP), in which it may serve as a retrograde messenger after postsynaptic NMDA receptor activation. In accordance with a prediction of this hypothesis, and with previous findings using guinea pig tissue, exogenous NO, when paired with a short tetanus (ST) to afferent fibers, generated a stable NMDA receptor-independent potentiation of rat CA1 hippocampal synaptic transmission that occluded LTP. Contrary to predictions, however, the pairing-induced potentiation was abolished in the presence of NO synthase inhibitors, indicating that endogenous NO is required for exogenous NO to facilitate LTP. Periodic application of NO while endogenous NO synthesis was blocked indicated that a tonic low level is necessary on both sides of the NO-ST pairing for the plasticity to occur. A similar dependence on tonic NO seems to extend to LTP, because application of an NO synthase inhibitor 5 min after tetanic stimulation blocked LTP as effectively as adding it beforehand. The posttetanus time window during which NO operated was restricted to <15 min. Inhibition of the guanylyl cyclase-coupled NO receptor indicated that the potentiation resulting from NO-ST pairing and the NO signal transduction pathway during early LTP are both through cGMP. We conclude that NO does not function simply as an acute signaling molecule in LTP induction but has an equally important role outside this phase. The results resonate with observations concerning the role of the hippocampal NO-cGMP pathway in certain types of learning behavior.
Key words: nitric oxide; hippocampus; long-term potentiation; guanylyl cyclase; cGMP; synaptic plasticity
Copyright © 2003 Society for Neuroscience 0270-6474/03/2351941-08$05.00/0
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