A requirement for the intercellular messenger nitric oxide in long-term potentiation.

Long-term potentiation (LTP) of synaptic transmission is a widely studied model of neuronal plasticity. The induction of LTP is known to require processes in the postsynaptic neuron, while experimental evidence suggests that the expression of LTP may occur in the presynaptic terminal. This has led to speculation that a retrograde messenger travels from the post- to the presynaptic cell during induction of LTP. Extracellular application or postsynaptic injection of two inhibitors of nitric oxide synthase, N-nitro-L-arginine or NG-methyl-L-arginine, blocks LTP. Extracellular application of hemoglobin, which binds nitric oxide, also attenuates LTP. These findings suggest that nitric oxide liberated from postsynaptic neurons may travel back to presynaptic terminals to cause LTP expression.

[1]  G. Lynch,et al.  Intracellular injections of EGTA block induction of hippocampal long-term potentiation , 1983, Nature.

[2]  Stephen J. Smith,et al.  NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones , 1986, Nature.

[3]  H. Wigström,et al.  Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. , 1986, Acta physiologica Scandinavica.

[4]  S. Kelso,et al.  Hebbian synapses in hippocampus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Lynch,et al.  Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. , 1986, Science.

[6]  B. R. Sastry,et al.  Associative induction of posttetanic and long-term potentiation in CA1 neurons of rat hippocampus. , 1986, Science.

[7]  S. Moncada,et al.  Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor , 1987, Nature.

[8]  C. Stevens,et al.  Glutamate activates multiple single channel conductances in hippocampal neurons , 1987, Nature.

[9]  G Lynch,et al.  Long-term potentiation differentially affects two components of synaptic responses in hippocampus. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[10]  C. Stevens.  A relaxing factor in the brain , 1988, Nature.

[11]  S. Moncada,et al.  L-arginine is the physiological precursor for the formation of nitric oxide in endothelium-dependent relaxation. , 1988, Biochemical and biophysical research communications.

[12]  C. Nathan,et al.  Identification of arginine as a precursor of endothelium-derived relaxing factor. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R S Zucker,et al.  Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. , 1988, Science.

[14]  R. Nicoll,et al.  A persistent postsynaptic modification mediates long-term potentiation in the hippocampus , 1988, Neuron.

[15]  M. Kennedy.  Synaptic memory molecules , 1988, Nature.

[16]  J. Garthwaite,et al.  Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain , 1988, Nature.

[17]  J. W. Goh,et al.  A pertussis toxin-sensitive G protein in hippocampal long-term potentiation. , 1989, Science.

[18]  S Moncada,et al.  Biosynthesis of nitric oxide from L-arginine. A pathway for the regulation of cell function and communication. , 1989, Biochemical pharmacology.

[19]  Richard Graham Knowles,et al.  Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[20]  B. Brüne,et al.  Activation of a cytosolic ADP-ribosyltransferase by nitric oxide-generating agents. , 1989, The Journal of biological chemistry.

[21]  T. Bliss,et al.  Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus , 1989, Nature.

[22]  S. Snyder,et al.  Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[23]  The tide of memory, turning. , 1990, Science.

[24]  C. Stevens,et al.  Presynaptic mechanism for long-term potentiation in the hippocampus , 1990, Nature.

[25]  T. Bliss.  Maintenance is presynaptic , 1990, Nature.

[26]  S. Snyder,et al.  Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[27]  C. Nathan,et al.  Does endothelium-derived nitric oxide have a role in cytokine-induced hypotension? , 1990, Journal of the National Cancer Institute.

[28]  S. Snyder,et al.  Localization of nitric oxide synthase indicating a neural role for nitric oxide , 1990, Nature.

[29]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[30]  B. McNaughton,et al.  Long‐term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content , 1991, Hippocampus.

[31]  S. Snyder,et al.  Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase , 1991, Nature.

[32]  R. Malinow.  Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. , 1991, Science.

[33]  S. Snyder,et al.  Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase , 1991, Neuron.

[34]  J. Vane,et al.  Involvement of nitric oxide in the reflex relaxation of the stomach to accommodate food or fluid , 1991, Nature.

[35]  G. Böhme,et al.  Possible involvement of nitric oxide in long-term potentiation. , 1991, European journal of pharmacology.

[36]  K. Shibuki,et al.  Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum , 1991, Nature.