Nitric Oxide Acts Directly in the Presynaptic Neuron to Produce Long-Term Potentiationin Cultured Hippocampal Neurons
Open accessAbstract
Nitric oxide (NO) has been proposed to act as a retrograde messenger during long-term potentiation (LTP) in the CA1 region of hippocampus, but the inaccessibility of the presynaptic terminal has prevented a definitive test of this hypothesis. Because both sides of the synapse are accessible in cultured hippocampal neurons, we have used this preparation to investigate the role of NO. We examined LTP following intra- or extracellular application of an NO scavenger, an inhibitor of NO synthase, and a membrane-impermeant NO donor that releases NO only upon photolysis with UV light. Our results indicate that NO is produced in the postsynaptic neuron, travels through the extracellular space, and acts directly in the presynaptic neuron to produce long-term potentiation, supporting the hypothesis that NO acts as a retrograde messenger during LTP.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Diverse mechanisms like retrograde signals using cannabinoids, or rapidly-diffusing gases such as nitric oxide, are among many that could enable learning rules that go beyond conventional conceptions of backpropagation.
“Beyond dendritic computation, diverse mechanisms (Marblestone and Boyden, 2014) like retrograde (post-synaptic to pre-synaptic) signals using cannabinoids (Wilson and Nicoll, 2001), or rapidly-diffusing gases such as nitric oxide (Arancio et al., 1996), are among many that could enable learning rules that go beyond conventional conceptions of backpropagation.”
From Toward an integration of deep learning and neuroscience (2016) · cites this paper as Arancio et al., 1996
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Liao, D., Hessler, N. A., & Malinow, R. (1995) · Nature · doi:10.1038/375400a0 · Cited by 1,365 · see citing works
Evidence for silent synapses: Implications for the expression of LTP
Isaac, J. T. R., Nicoll, R. A., & Malenka, R. C. (1995) · Neuron · doi:10.1016/0896-6273(95)90046-2 · Cited by 1,233 · see citing works
A Requirement for the Intercellular Messenger Nitric Oxide in Long-Term Potentiation
Schuman, E. M., & Madison, D. V. (1991) · Science · doi:10.1126/science.1720572 · Cited by 1,135 · see citing works
O’Dell, T. J., Hawkins, R. D., Kandel, E. R., & Arancio, O. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.24.11285 · Cited by 1,034 · see citing works
Self-citationPresynaptic mechanism for long-term potentiation in the hippocampus
Bekkers, J. M., & Stevens, C. F. (1990) · Nature · doi:10.1038/346724a0 · Cited by 690 · see citing works
Possible involvement of nitric oxide in long-term potentiation
Böhme, G. A., Bon, C. L. M., Stutzmann, J. M., Doble, A., & Blanchard, J. (1991) · European Journal of Pharmacology · doi:10.1016/0014-2999(91)90505-k · Cited by 632 · see citing works
Hebbian synapses in hippocampus.
Kelso, S. R., Ganong, A. H., & Brown, T. H. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.14.5326 · Cited by 555 · see citing works
Zhuo, M., Small, S. A., Kandel, E. R., & Hawkins, R. D. (1993) · Science · doi:10.1126/science.8100368 · Cited by 553 · see citing works
Self-citationA Text-book of Quantitative Chemical Analysis
Cumming, A. C., & Kay, S. A. (1923) · Nature · doi:10.1038/111321c0 · Cited by 512 · see citing works
The role of nitric oxide in hippocampal long-term potentiation
Haley, J. E., Wilcox, G. L., & Chapman, P. F. (1992) · Neuron · doi:10.1016/0896-6273(92)90288-o · Cited by 470 · see citing works
The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture
Fletcher, T., Cameron, P. L., Camilli, P. V. D., & Banker, G. A. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-06-01617.1991 · Cited by 454 · see citing works
Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation
Zhuo, M., Hu, Y., Schultz, C., Kandel, E. R., & Hawkins, R. D. (1994) · Nature · doi:10.1038/368635a0 · Cited by 440 · see citing works
Self-citationSon, H., Hawkins, R. D., Martin, K. C., Kiebler, M. A., Huang, P. L., Fishman, M. C., & Kandel, E. R. (1996) · Cell · doi:10.1016/s0092-8674(00)81796-1 · Cited by 429 · see citing works
Self-citationLearning to modulate transmitter release: themes and variations in synaptic plasticity.
Hawkins, R. D., Kandel, E., & Siegelbaum, S. (1993) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.16.030193.003205 · Cited by 404 · see citing works
Self-citationMalgaroli, A., & Tsien, R. (1992) · Nature · doi:10.1038/357134a0 · Cited by 384 · see citing works
Self-citationArancio, O., Kandel, E. R., & Hawkins, R. D. (1995) · Nature · doi:10.1038/376074a0 · Cited by 301 · see citing works
Self-citationEast, S. J., & Garthwaite, J. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90147-l · Cited by 295 · see citing works
Reversal of long-term potentiation by inhibitors of haem oxygenase
Stevens, C. F., & Wang, Y. (1993) · Nature · doi:10.1038/364147a0 · Cited by 262 · see citing works
Lev‐Ram, V., Makings, L. R., Keitz, P. F., Kao, J. P. Y., & Tsien, R. Y. (1995) · Neuron · doi:10.1016/0896-6273(95)90044-6 · Cited by 236 · see citing works
Self-citationNitric Oxide Modulates Synaptic Vesicle Docking/Fusion Reactions
Meffert, M. K., Calakos, N., Scheller, R. H., & Schulman, H. (1996) · Neuron · doi:10.1016/s0896-6273(00)80149-x · Cited by 227 · see citing works
Schuman, E. M., Meffert, M. K., Schulman, H., & Madison, D. V. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.25.11958 · Cited by 139 · see citing works
The Nitric Oxide ‐ Cyclic GMP Pathway and Synaptic Depression in Rat Hippocampal Slices
Boulton, C. L., Irving, A. J., Southam, E., Potier, B., Garthwaite, J., & Collingridge, G. L. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00543.x · Cited by 137 · see citing works
Nanomolar NG-nitroarginine inhibits NMDA-induced cyclic GMP formation in rat cerebellum
East, S. J., & Garthwaite, J. (1990) · European Journal of Pharmacology · doi:10.1016/0014-2999(90)90623-e · Cited by 133 · see citing works
Caged nitric oxide. Stable organic molecules from which nitric oxide can be photoreleased.
Makings, L. R., & Tsien, R. Y. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37368-4 · Cited by 125 · see citing works
Self-citationGorbunov, N. V., Osipov, A. N., Day, B. W., Zayas-Rivera, B., Kagan, V. E., & Elsayed, N. M. (1995) · Biochemistry · doi:10.1021/bi00020a014 · Cited by 123 · see citing works
Diffusional transport of macromolecules in developing nerve processes
Popov, S., & Poo, M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-01-00077.1992 · Cited by 120 · see citing works
Hawkins, R. D. (1996) · Neuron · doi:10.1016/s0896-6273(00)80064-1 · Cited by 92 · see citing works
Self-citationMurphy, K., Williams, J. H. H., Bettache, N., & Bliss, T. V. P. (1994) · Neuropharmacology · doi:10.1016/0028-3908(94)90039-6 · Cited by 66 · see citing works
Retrograde signaling at the synapse
Murphey, R. K., & Davis, G. W. (1994) · Journal of Neurobiology · doi:10.1002/neu.480250602 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD).
Luscher, C., & Malenka, R. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005710 · Cited by 1,110 · see citing works
Nitric oxide as modulator of neuronal function
Prast, H., & Philippu, A. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00044-7 · Cited by 937 · see citing works
Nitric oxide signaling in health and disease
Lundberg, J. O., & Weitzberg, E. (2022) · Cell · doi:10.1016/j.cell.2022.06.010 · Cited by 850 · see citing works
(S)NO Signals: Translocation, Regulation, and a Consensus Motif
Stamler, J. S., Toone, E. J., Lipton, S. A., & Sucher, N. J. (1997) · Neuron · doi:10.1016/s0896-6273(00)80310-4 · Cited by 674 · see citing works
The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents
Dere, E., Huston, J. P., & Silva, M. A. D. S. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.005 · Cited by 669 · see citing works
Silent synapses and the emergence of a postsynaptic mechanism for LTP
Kerchner, G. A., & Nicoll, R. A. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2501 · Cited by 602 · see citing works
Insulin and the insulin receptor in experimental models of learning and memory
Zhao, W., Chen, H., Quon, M. J., & Alkon, D. L. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.045 · Cited by 503 · see citing works
Son, H., Hawkins, R. D., Martin, K. C., Kiebler, M. A., Huang, P. L., Fishman, M. C., & Kandel, E. R. (1996) · Cell · doi:10.1016/s0092-8674(00)81796-1 · Cited by 429 · see citing works
Self-citationNitric Oxide Signaling Contributes to Late-Phase LTP and CREB Phosphorylation in the Hippocampus
Lü, Y.-F., Kandel, E. R., & Hawkins, R. D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10250.1999 · Cited by 409 · see citing works
Self-citationNitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity
Hölscher, C. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01065-5 · Cited by 408 · see citing works
Functions and dysfunctions of nitric oxide in brain
Picón-Pagès, P., Garcia-Buendia, J., & Muñoz, F. J. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.11.007 · Cited by 357 · see citing works
Long-term potentiation: What's learning got to do with it?
Shors, T. J., & Matzel, L. D. (1997) · Behavioral and Brain Sciences · doi:10.1017/s0140525x97001593 · Cited by 314 · see citing works
SENSITIZATION OF PAIN PATHWAYS IN THE SPINAL CORD: CELLULAR MECHANISMS
Baranauskas, G., & Nistri, A. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00067-1 · Cited by 295 · see citing works
Chapter 11 Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus
Hawkins, R. D., Son, H., & Arancio, O. (1998) · Progress in brain research · doi:10.1016/s0079-6123(08)63206-9 · Cited by 271 · see citing works
Self-citationFuentealba, P., Begum, R., Capogna, M., Jinno, S., Márton, L. F., Csicsvari, J., Thomson, A., Somogyi, P., & Klausberger, T. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.034 · Cited by 255 · see citing works
Formation of olfactory memories mediated by nitric oxide
Kendrick, K. M., Guevara‐Guzmán, R., Zorrilla, J., Hinton, M. R., Broad, K. D., Mimmack, M. L., & Ohkura, S. (1997) · Nature · doi:10.1038/41765 · Cited by 264 · see citing works
The role of nitric oxide in pre-synaptic plasticity and homeostasis
Hardingham, N. R., Dachtler, J., & Fox, K. D. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00190 · Cited by 260 · see citing works
Lev‐Ram, V., Jiang, T., Wood, J. S., Lawrence, D. S., & Tsien, R. Y. (1997) · Neuron · doi:10.1016/s0896-6273(00)80340-2 · Cited by 260 · see citing works
Self-citationSynapse specificity of long-term potentiation breaks down at short distances
Engert, F., & Bonhoeffer, T. (1997) · Nature · doi:10.1038/40870 · Cited by 252 · see citing works
Puzzo, D., Vitolo, O. V., Trinchese, F., Jacob, J. P., Palmeri, A., & Arancio, O. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5291-04.2005 · Cited by 243 · see citing works
Self-citationEpisodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory
Dere, E., Huston, J. P., & Silva, M. A. D. S. (2005) · Brain Research Protocols · doi:10.1016/j.brainresprot.2005.08.001 · Cited by 242 · see citing works
Tonic and phasic nitric oxide signals in hippocampal long-term potentiation
Hopper, R. A., & Garthwaite, J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2259-06.2006 · Cited by 239 · see citing works
Molecular Mechanisms of Memory Storage inAplysia
Hawkins, R. D., Kandel, E. R., & Bailey, C. H. (2006) · Biological Bulletin · doi:10.2307/4134556 · Cited by 231 · see citing works
Self-citationWang, H., Lu, F.-M., Jin, I., Udo, H., Kandel, E. R., de Vente, J., Walter, U., Lohmann, S. M., Hawkins, R. D., & Antonova, I. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.011 · Cited by 216 · see citing works
Self-citationTrinchese, F., Fà, M., Liu, S., Zhang, H., Hidalgo, A., Schmidt, S. D., Yamaguchi, H., Yoshii, N., Mathews, P. M., Nixon, R. A., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34254 · Cited by 205 · see citing works
Self-citationα‐Synuclein produces a long‐lasting increase in neurotransmitter release
Liu, S., Ninan, I., Antonova, I., Battaglia, F., Trinchese, F., Narasanna, A., Kolodilov, N., Dauer, W., Hawkins, R. D., & Arancio, O. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600451 · Cited by 198 · see citing works
Self-citationSynaptic Localization of Nitric Oxide Synthase and Soluble Guanylyl Cyclase in the Hippocampus
Burette, A., Zabel, U., Weinberg, R. J., Schmidt, H. H. H. W., & Valtschanoff, J. G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-20-08961.2002 · Cited by 196 · see citing works
NO/cGMP-Dependent Modulation of Synaptic Transmission
Feil, R., & Kleppisch, T. (2007) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-74805-2_16 · Cited by 190 · see citing works
Nitric oxide mediates N -methyl- d -aspartate receptor-induced activation of p21 ras
Yun, H., Gonzalez‐Zulueta, M., Dawson, V. L., & Dawson, T. M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.10.5773 · Cited by 190 · see citing works
Nitric oxide and neurological disorders
Duncan, A., & Heales, S. (2005) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2004.09.004 · Cited by 189 · see citing works
Modulation of oxidative stress and mitochondrial function by the ketogenic diet
Milder, J. B., & Patel, M. (2011) · Epilepsy Research · doi:10.1016/j.eplepsyres.2011.09.021 · Cited by 181 · see citing works
Kumar, A. (2011) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2011.00007 · Cited by 169 · see citing works
Susswein, A. J., Katzoff, A., Miller, N., & Hurwitz, I. (2004) · The Neuroscientist · doi:10.1177/1073858403261226 · Cited by 166 · see citing works
cGMP Signalling in the Mammalian Brain: Role in Synaptic Plasticity and Behaviour
Kleppisch, T., & Feil, R. (2009) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-540-68964-5_24 · Cited by 161 · see citing works
Presynaptic Role of cGMP-Dependent Protein Kinase during Long-Lasting Potentiation
Arancio, O., Antonova, I., Gambaryan, S. P., Lohmann, S. M., Wood, J. S., Lawrence, D. S., & Hawkins, R. D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00143.2001 · Cited by 161 · see citing works
Self-citationHeterocyclic N-Oxides - An Emerging Class of Therapeutic Agents
Mfuh, A. M., & Larionov, O. V. (2015) · Current Medicinal Chemistry · doi:10.2174/0929867322666150619104007 · Cited by 159 · see citing works
Lü, Y.-F., & Hawkins, R. D. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.3.1270 · Cited by 153 · see citing works
Self-citationRetrograde signaling at central synapses
Tao, H. W., & Poo, M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191351698 · Cited by 138 · see citing works
Presynaptic long-term plasticity
Yang, Y., & Calakos, N. (2013) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2013.00008 · Cited by 135 · see citing works
Mustafa, A. K., Kumar, M., Selvakumar, B., Ho, G. P. H., Ehmsen, J. T., Barrow, R. K., Amzel, L. M., & Snyder, S. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611620104 · Cited by 136 · see citing works
Sola, E., Prestori, F., Rossi, P., Taglietti, V., & D'Angelo, E. (2004) · Journal of Physiology · doi:10.1113/jphysiol.2003.060285 · Cited by 161 · see citing works
The past, the future and the biology of memory storage
Kandel, E. R., & Pittenger, C. (1999) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1999.0542 · Cited by 134 · see citing works
Self-citationOta, K. T., Pierre, V. J., Ploski, J. E., Queen, K., & Schafe, G. E. (2008) · Learning & Memory · doi:10.1101/lm.1114808 · Cited by 133 · see citing works
Nitric oxide signaling in invertebrates
Jacklet, J. W. (1997) · Invertebrate Neuroscience · doi:10.1007/bf02481710 · Cited by 128 · see citing works
The Specific Role of cGMP in Hippocampal LTPPreprint
Son, H., Lü, Y.-F., Zhuo, M., Arancio, O., Kandel, E. R., & Hawkins, R. D. (1998) · Learning & Memory · doi:10.1101/lm.5.3.231 · Cited by 129 · see citing works
Self-citationPresynaptic CaMKII Is Necessary for Synaptic Plasticity in Cultured Hippocampal Neurons
Ninan, I., & Arancio, O. (2004) · Neuron · doi:10.1016/s0896-6273(04)00143-6 · Cited by 120 · see citing works
Self-citationToward an integration of deep learning and neuroscience
Marblestone, A. H., Wayne, G., & Kording, K. P. (2016) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2016.00094 · Cited by 119 · see citing works
Blackshaw, S., Eliasson, M. J. L., Sawa, A., Watkins, C. C., Krug, D. K., Gupta, A., Arai, T., Ferrante, R. J., & Snyder, S. H. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00217-3 · Cited by 116 · see citing works
Kleppisch, T., Pfeifer, A., Klatt, P., Ruth, P., Montkowski, A., Fässler, R., & Hofmann, F. B. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00048.1999 · Cited by 115 · see citing works
Effects of Nitric Oxide on Neuroendocrine Function and Behavior
Nelson, R. J., Kriegsfeld, L. J., Dawson, V. L., & Dawson, T. M. (1997) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1997.0156 · Cited by 113 · see citing works
Transcription‐dependent neuronal plasticity
Bading, H. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2000.01565.x · Cited by 112 · see citing works
Cyclic nucleotide gated channels as regulators of CNS development and plasticity
Zufall, F., Shepherd, G. M., & Barnstable, C. J. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80070-0 · Cited by 112 · see citing works
Zhang, C., Czymmek, K. J., & Shapiro, A. D. (2003) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2003.16.11.962 · Cited by 112 · see citing works
Activation of NF- κ B by Reactive Oxygen Intermediates in the Nervous System
Kaltschmidt, B., Sparna, T., & Kaltschmidt, C. (1999) · Antioxidants and Redox Signaling · doi:10.1089/ars.1999.1.2-129 · Cited by 110 · see citing works
Synaptic plasticity: A role for nitric oxide in LTP
Huang, E. P. (1997) · Current Biology · doi:10.1016/s0960-9822(97)70073-3 · Cited by 110 · see citing works
Bao, J., Kandel, E. R., & Hawkins, R. D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00458.1998 · Cited by 109 · see citing works
Self-citationKo, G. Y. ‐., & Kelly, P. T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-06784.1999 · Cited by 108 · see citing works
Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation
Bayazitov, I. T., Richardson, R. J., Fricke, R. G., & Zakharenko, S. S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3077-07.2007 · Cited by 102 · see citing works
Apergis-Schoute, A. M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0096-05.2005 · Cited by 101 · see citing works
Effects of nitric oxide synthase gene knockout on neurotransmitter release in vivo
Kano, T., Shimizu‐Sasamata, M., Huang, P. L., Moskowitz, M. A., & Lo, E. H. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00179-1 · Cited by 103 · see citing works
Is the Amyloid Hypothesis of Alzheimer's disease therapeutically relevant?
Teich, A. F., & Arancio, O. (2012) · Biochemical Journal · doi:10.1042/bj20120653 · Cited by 102 · see citing works
Self-citationNitrosative stress in Parkinson’s disease
Stykel, M. G., & Ryan, S. D. (2022) · npj Parkinson s Disease · doi:10.1038/s41531-022-00370-3 · Cited by 97 · see citing works
Mouse Chromaffin Cells Have Two Populations of Dense Core Vesicles
Grabner, C. P., Price, S. D., Lysakowski, A., & Fox, A. P. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00316.2005 · Cited by 96 · see citing works
Ledo, A., Barbosa, R. M., Gerhardt, G. A., Cadenas, E., & Laranjinha, J. A. N. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503624102 · Cited by 97 · see citing works
Jacoby, S., Sims, R. E., & Hartell, N. A. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.t01-1-00825.x · Cited by 97 · see citing works
Role of phosphodiesterase 5 in synaptic plasticity and memory
Puzzo, D. (2008) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s2447 · Cited by 94 · see citing works
Structure and projections of white matter neurons in the postnatal rat visual cortex
Clancy, B., Silva‐Filho, M., & Friedlander, M. J. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1174 · Cited by 94 · see citing works
Development of novel phosphodiesterase 5 inhibitors for the therapy of Alzheimer’s disease
Zuccarello, E., Acquarone, E., Calcagno, E., Argyrousi, E. K., Deng, S., Landry, D. W., Arancio, O., & Fiorito, J. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.113818 · Cited by 93 · see citing works
Self-citationKlotho Is a Neuroprotective and Cognition-Enhancing Protein
Abraham, C. R., Mullen, P., Zhou, T. B. T., Chen, C.-D., & Zeldich, E. (2016) · Vitamins and hormones · doi:10.1016/bs.vh.2016.02.004 · Cited by 92 · see citing works
Schafe, G. E., Bauer, E. P., Rosis, S., Farb, C. R., Rodrigues, S. M., & LeDoux, J. E. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04209.x · Cited by 92 · see citing works
Kleppisch, T., Wolfsgruber, W., Feil, S. C., Allmann, R., Wotjak, C. T., Goebbels, S., Nave, K., Hofmann, F. B., & Feil, R. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-14-06005.2003 · Cited by 91 · see citing works
Glutamate receptors and signal transduction in learning and memory
Peng, S., Zhang, Y., Zhang, J., Wang, H., & Ren, B. (2010) · Molecular Biology Reports · doi:10.1007/s11033-010-0128-9 · Cited by 89 · see citing works
Taqatqeh, F., Mergia, E., Neitz, A., Eysel, U. T., Koesling, D., & Mittmann, T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1902-09.2009 · Cited by 88 · see citing works
Sources and targets of nitric oxide signalling in insect nervous systems
Bicker, G. (2001) · Cell and Tissue Research · doi:10.1007/s004410000321 · Cited by 88 · see citing works
Conditioning Method Dramatically Alters the Role of Amygdala in Taste Aversion LearningPreprint
Schafe, G. E., Thiele, T. E., & Bernstein, I. L. (1998) · Learning & Memory · doi:10.1101/lm.5.6.481 · Cited by 85 · see citing works
Furoxans (1,2,5-Oxadiazole- N -Oxides) as Novel NO Mimetic Neuroprotective and Procognitive Agents
Schiefer, I. T., VandeVrede, L. A., Fà, M., Arancio, O., & Thatcher, G. R. J. (2012) · Journal of Medicinal Chemistry · doi:10.1021/jm201504s · Cited by 84 · see citing works
Self-citationIsoflurane inhibits the neurotransmitter release machinery
Herring, B. E., Xie, Z., Marks, J., & Fox, A. P. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00252.2009 · Cited by 83 · see citing works
Haul, S., Gödecke, A., Schrader, J., Haas, H. L., & Luhmann, H. J. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.2.494 · Cited by 82 · see citing works
Harooni, H. E., Naghdi, N., Sepehri, H., & Rohani, A. H. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.02.011 · Cited by 81 · see citing works
Grassi, S., & Pettorossi, V. E. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00070-8 · Cited by 81 · see citing works
Endogenous formaldehyde is a memory-related molecule in mice and humans
Ai, L., Tan, T., Tang, Y., Yang, J., Cui, D., Wang, R., Wang, A., Fei, X., Di, Y., Wang, X., et al. (2019) · Communications Biology · doi:10.1038/s42003-019-0694-x · Cited by 81 · see citing works
Dual role of nitric oxide in Alzheimer's disease
Azargoonjahromi, A. (2023) · Nitric Oxide · doi:10.1016/j.niox.2023.03.003 · Cited by 83 · see citing works
Ota, K. T., Monsey, M. S., Wu, M. S., & Schafe, G. E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011236 · Cited by 80 · see citing works
Unni, V. K., Zakharenko, S. S., Zablow, L., DeCostanzo, A. J., & Siegelbaum, S. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5583-03.2004 · Cited by 78 · see citing works
Nitric oxide in brain: diffusion, targets and concentration dynamics in hippocampal subregions
Ledo, A., Frade, J. G., Barbosa, R. M., & Laranjinha, J. A. N. (2004) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2004.02.010 · Cited by 77 · see citing works
Cellular and molecular bases of memory: synaptic and neuronal plasticity.
Wang, J.-H., Ko, G., & Kelly, P. T. (1997) · Journal of clinical neurophysiology · doi:10.1097/00004691-199707000-00002 · Cited by 79 · see citing works
Bicker, G. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01236-3 · Cited by 76 · see citing works
Two sides to long-term potentiation: a view towards reconciliation
Padamsey, Z., & Emptage, N. J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0154 · Cited by 75 · see citing works
Sildenafil Improves Vascular and Metabolic Function in Patients with Alzheimer’s Disease
Sheng, M., Lu, H., Liu, P., Li, Y., Ravi, H., Peng, S., Diaz-Arrastia, R. R., Devous, M. D., & Womack, K. B. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161006 · Cited by 75 · see citing works
cGMP-Mediated Facilitation in Nerve Terminals by Enhancement of the Spike Afterhyperpolarization
Klyachko, V. A., Ahern, G. P., & Jackson, M. B. (2001) · Neuron · doi:10.1016/s0896-6273(01)00449-4 · Cited by 74 · see citing works
Emerging Roles of Endothelial Nitric Oxide in Preservation of Cognitive Health
Katusic, Z. S., d’Uscio, L. V., & He, T. (2023) · Stroke · doi:10.1161/strokeaha.122.041444 · Cited by 73 · see citing works
Effects of molsidomine on scopolamine-induced amnesia and hypermotility in the rat
Pitsikas, N., Rigamonti, A. E., Cella, S. G., Locatelli, V., Sala, M., & Müller, E. E. (2001) · European Journal of Pharmacology · doi:10.1016/s0014-2999(01)01164-5 · Cited by 73 · see citing works
Selective Presynaptic Propagation of Long-Term Potentiation in Defined Neural Networks
Tao, H. W., Zhang, L. I., Bi, G., & Poo, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-09-03233.2000 · Cited by 73 · see citing works
Involvement of Reactive Oxygen Species in Long-Term Potentiation in the Spinal Cord Dorsal Horn
Lee, K. Y., Chung, K., & Chung, J. M. (2009) · Journal of Neurophysiology · doi:10.1152/jn.90906.2008 · Cited by 72 · see citing works
Learning and Memory: Basic Mechanisms
Byrne, J., LaBar, K., LeDoux, J. E., Schafe, G., & Thompson, R. F. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397179-1.00020-8 · Cited by 27 · see citing works
Rosa, G. D., Odrlijn, T., Nixon, R. A., & Arancio, O. (2002) · Journal of Molecular Neuroscience · doi:10.1007/s12031-002-0024-4 · Cited by 71 · see citing works
Self-citationMattson, M. P. (1998) · International review of neurobiology · doi:10.1016/s0074-7742(08)60609-1 · Cited by 69 · see citing works
Long-Term Potentiation in the Visual Cortex Requires Both Nitric Oxide Receptor Guanylyl Cyclases
Haghikia, A., Mergia, E., Friebe, A., Eysel, U. T., Koesling, D., & Mittmann, T. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4706-06.2007 · Cited by 70 · see citing works
Kimura, S., Uchiyama, S., Takahashi, H. E., & Shibuki, K. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08551.1998 · Cited by 68 · see citing works
Acquarone, E., Argyrousi, E. K., van den Berg, M., Gulisano, W., Fà, M., Staniszewski, A., Calcagno, E., Zuccarello, E., D'adamio, L., Deng, S.-X., et al. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0326-4 · Cited by 67 · see citing works
Self-citation
- Authors
- Arancio, O., Kiebler, M., Lee, C. J., Lev-Ram, V., Tsien, R. Y., Kandel, E. R., & Hawkins, R. D.
- Affiliations
- Columbia University (US)
- Howard Hughes Medical Institute (US)
- New York State Psychiatric Institute (US)
- Corresponding author
- Hawkins, Robert D
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 1996-12
- Volume
- 87
- Issue
- 6
- Pages
- 1025-1035
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2102133195
- Cited by
- 357
- References
- 30
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 7 · 2023: 8 · 2022: 10 · 2021: 7 · 2020: 8 · 2019: 8 · 2018: 7 · 2017: 7 · 2016: 6 · 2015: 5 · 2014: 14 · 2013: 13 · 2012: 11
- FWCI
- 8.37
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (P50MH050733, MH-50733)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Keywords
- nitric oxide, long-term potentiation, retrograde signaling, presynaptic neurons, hippocampal neurons, NO synthase inhibition, NO scavenger, CA1 region
- MeSH terms
- Animals, Cells, Cultured, Extracellular Space, Fluorescent Antibody Technique, Hippocampus, Membrane Potentials, Methemoglobin, Microinjections, Myoglobin, Neurons, Nitric Oxide, Photolysis, Tetanus Toxin, Ultraviolet Rays, Rats, Sprague-Dawley, Presynaptic Terminals, Long-Term Potentiation, Neurotransmitter Agents, Nitric Oxide Synthase, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review