Emotion Enhances Learning via Norepinephrine Regulation of AMPA-Receptor Trafficking
Open accessAbstract
Emotion enhances our ability to form vivid memories of even trivial events. Norepinephrine (NE), a neuromodulator released during emotional arousal, plays a central role in the emotional regulation of memory. However, the underlying molecular mechanism remains elusive. Toward this aim, we have examined the role of NE in contextual memory formation and in the synaptic delivery of GluR1-containing alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid (AMPA)-type glutamate receptors during long-term potentiation (LTP), a candidate synaptic mechanism for learning. We found that NE, as well as emotional stress, induces phosphorylation of GluR1 at sites critical for its synaptic delivery. Phosphorylation at these sites is necessary and sufficient to lower the threshold for GluR1 synaptic incorporation during LTP. In behavioral experiments, NE can lower the threshold for memory formation in wild-type mice but not in mice carrying mutations in the GluR1 phosphorylation sites. Our results indicate that NE-driven phosphorylation of GluR1 facilitates the synaptic delivery of GluR1-containing AMPARs, lowering the threshold for LTP, thereby providing a molecular mechanism for how emotion enhances learning and memory.
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High levels of noradrenaline acting at α1- and β-receptors enhance memory consolidation processes in the hippocampus and increase the signal/noise ratio in primary sensory cortices.
“For example, high levels of noradrenaline acting at α1- and β-receptors enhance memory consolidation processes in the hippo-campus82,83 and increase the signal/noise ratio in primary sensory cortices84–86.”
From Stress signalling pathways that impair prefrontal cortex structure and function (2009) · cites this paper as [83]
No passage from our copy was returned for hippocampal memory consolidation, α1- or β-adrenergic receptors, or signal-to-noise ratio in sensory cortex. Searches for “hippocampus,” “memory consolidation,” “adrenergic,” and “sensory” also returned no passages, so there is no section or page on which to assess the attribution. (LLM, conf=0.70)
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Cites
(1982) · Trends in Neurosciences · doi:10.1016/0166-2236(82)90076-5 · Cited by 9,148 · see citing works
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Self-citationA cognitive model of posttraumatic stress disorder
Ehlers, A., & Clark, D. M. (2000) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(99)00123-0 · Cited by 6,147 · see citing works
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · see citing works
Hollmann, M., & Heinemann, S. F. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.000335 · Cited by 4,011 · see citing works
Malenka, R. C., & Bear, M. F. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.012 · Cited by 3,968 · see citing works
Bienenstock, E., Cooper, L., & Munro, P. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-01-00032.1982 · Cited by 2,896 · see citing works
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
Self-citationNeurobiology of Pavlovian Fear Conditioning
Maren, S. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.897 · Cited by 1,805 · see citing works
Hayashi, Y., Shi, S.-H., Esteban, J. A., Piccini, A., Poncer, J.-C., & Malinow, R. (2000) · Science · doi:10.1126/science.287.5461.2262 · Cited by 1,524 · see citing works
Self-citationRapid Spine Delivery and Redistribution of AMPA Receptors After Synaptic NMDA Receptor Activation
Shi, S.-H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K., & Malinow, R. (1999) · Science · doi:10.1126/science.284.5421.1811 · Cited by 1,276 · see citing works
Self-citationβ-Adrenergic activation and memory for emotional events
Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994) · Nature · doi:10.1038/371702a0 · Cited by 1,271 · see citing works
AMPA receptor trafficking at excitatory synapses
Bredt, D. S., & Nicoll, R. A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00640-8 · Cited by 1,150 · see citing works
Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity
Lee, H.-K., Barbarosie, M., Kameyama, K., Bear, M. F., & Huganir, R. L. (2000) · Nature · doi:10.1038/35016089 · Cited by 1,116 · see citing works
Self-citationStargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms
Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., Bredt, D. S., & Nicoll, R. A. (2000) · Nature · doi:10.1038/35050030 · Cited by 1,111 · see citing works
Reinsertion or Degradation of AMPA Receptors Determined by Activity-Dependent Endocytic Sorting
Ehlers, M. D. (2000) · Neuron · doi:10.1016/s0896-6273(00)00129-x · Cited by 1,096 · see citing works
Shi, S.-H., Hayashi, Y., Esteban, J. A., & Malinow, R. (2001) · Cell · doi:10.1016/s0092-8674(01)00321-x · Cited by 1,094 · see citing works
Self-citationRegulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation
Barria, A., Muller, D., Derkach, V., Griffith, L. C., & Soderling, T. R. (1997) · Science · doi:10.1126/science.276.5321.2042 · Cited by 1,049 · see citing works
Molecular Cloning and Functional Expression of Glutamate Receptor Subunit Genes
Boulter, J., Hollmann, M., O'Shea-Greenfield, A., Hartley, M., Deneris, E. S., Maron, C., & Heinemann, S. F. (1990) · Science · doi:10.1126/science.2168579 · Cited by 939 · see citing works
PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity
Esteban, J. A., Shi, S.-H., Wilson, C., Nuriya, M., Huganir, R. L., & Malinow, R. (2003) · Nature Neuroscience · doi:10.1038/nn997 · Cited by 894 · see citing works
Self-citationDerkach, V., Barria, A., & Soderling, T. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.6.3269 · Cited by 842 · see citing works
Role of adrenal stress hormones in forming lasting memories in the brain
McGaugh, J. L., & Roozendaal, B. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00306-9 · Cited by 818 · see citing works
Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit
Roche, K. W., O'Brien, R. J., Mammen, A. L., Bernhardt, J., & Huganir, R. L. (1996) · Neuron · doi:10.1016/s0896-6273(00)80144-0 · Cited by 812 · see citing works
Self-citationLee, H.-K., Takamiya, K., Han, J.-S., Man, H., Kim, C.-H., Rumbaugh, G., Yu, S., Ding, L., He, C., Petralia, R. S., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00122-3 · Cited by 802 · see citing works
Self-citationImportance of AMPA Receptors for Hippocampal Synaptic Plasticity But Not for Spatial Learning
Zamanillo, D., Sprengel, R., Hvalby, Ø., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K. M. M., Köster, H. J., Borchardt, T., Worley, P., et al. (1999) · Science · doi:10.1126/science.284.5421.1805 · Cited by 791 · see citing works
Regulation of AMPA receptors during synaptic plasticity
Song, I., & Huganir, R. L. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02270-1 · Cited by 777 · see citing works
Self-citationPostsynaptic receptor trafficking underlying a form of associative learning
Rumpel, S., LeDoux, J., Zador, A., & Malinow, R. (2005) · Science · doi:10.1126/science.1103944 · Cited by 775 · see citing works
Self-citationInvolvement of the amygdala in memory storage: Interaction with other brain systems
McGaugh, J. L., Cahill, L. F., & Roozendaal, B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13508 · Cited by 747 · see citing works
Contextual fear, gestalt memories, and the hippocampus.
Fanselow, M. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00186-2 · Cited by 724 · see citing works
Unusual spectral energy distribution of a galaxy previously reported to be at redshift 6.68
Chen, H., Lanzetta, K. M., Pascarelle, S. M., & Yahata, N. (2000) · RePEc: Research Papers in Economics · Cited by 680 · see citing works
Experience-dependent modification of synaptic plasticity in visual cortex
Kirkwood, A., Rioult, M., & Bear, M. (1996) · Nature · doi:10.1038/381526a0 · Cited by 666 · see citing works
Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase
Banke, T. G., Bowie, D., Lee, H.-K., Huganir, R. L., Schousboe, A., & Traynelis, S. F. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00089.2000 · Cited by 652 · see citing works
Self-citationNoradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus
Madison, D. V., & Nicoll, R. A. (1982) · Nature · doi:10.1038/299636a0 · Cited by 581 · see citing works
Bach, M. E., Hawkins, R. D., Osman, M., Kandel, E. R., & Mayford, M. R. (1995) · Cell · doi:10.1016/0092-8674(95)90010-1 · Cited by 475 · see citing works
Oh, M. C., Derkach, V. A., Guire, E. S., & Soderling, T. R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509677200 · Cited by 456 · see citing works
Mammen, A. L., Kameyama, K., Roche, K. W., & Huganir, R. L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.51.32528 · Cited by 441 · see citing works
Self-citationPostnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity
Zhu, J. J., Esteban, J. A., Hayashi, Y., & Malinow, R. (2000) · Nature Neuroscience · doi:10.1038/80614 · Cited by 437 · see citing works
Self-citationHaas, H. L., & Konnerth, A. (1983) · Nature · doi:10.1038/302432a0 · Cited by 413 · see citing works
Liang, K., Juler, R. G., & McGaugh, J. L. (1986) · Brain Research · doi:10.1016/0006-8993(86)91049-8 · Cited by 392 · see citing works
Boehm, J., Kang, M.-G., Johnson, R. C., Esteban, J., Huganir, R. L., & Malinow, R. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.013 · Cited by 382 · see citing works
Self-citationLeonard, A. S., Davare, M. A., Horne, M. C., Garner, C. C., & Hell, J. W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.31.19518 · Cited by 374 · see citing works
Spatial memory dissociations in mice lacking GluR1
Reisel, D., Bannerman, D. M., Schmitt, W. B., Deacon, R. M. J., Jonathan Flint, C., Borchardt, T., Seeburg, P. H., & Rawlins, J. N. P. (2002) · Nature Neuroscience · doi:10.1038/nn910 · Cited by 343 · see citing works
Mammalian ionotropic glutamate receptors
Wisden, W., & Seeburg, P. H. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90120-n · Cited by 322 · see citing works
Winder, D. G., Martin, K. C., Muzzio, I. A., Rohrer, D. K., Chruscinski, A. J., Kobilka, B. K., & Kandel, E. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)81124-1 · Cited by 321 · see citing works
Snyder, G. L., Allen, P. B., Fienberg, A. A., Valle, C. G., Huganir, R. L., Nairn, A. C., & Greengard, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-12-04480.2000 · Cited by 311 · see citing works
Self-citationReceptor trafficking and the plasticity of excitatory synapses
Barry, M. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00329-x · Cited by 307 · see citing works
Experience Strengthening Transmission by Driving AMPA Receptors into Synapses
Takahashi, T., Svoboda, K., & Malinow, R. (2003) · Science · doi:10.1126/science.1079886 · Cited by 306 · see citing works
Self-citationThe amygdala, fear, and memory
FANSELOW, M. S., & GALE, G. D. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07077.x · Cited by 299 · see citing works
Gray, R. G. F., & Johnston, D. (1987) · Nature · doi:10.1038/327620a0 · Cited by 285 · see citing works
Thomas, M. J., Moody, T. D., Makhinson, M., & O’Dell, T. J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80179-8 · Cited by 283 · see citing works
Kameyama, K., Lee, H.-K., Bear, M. F., & Huganir, R. L. (1998) · Neuron · doi:10.1016/s0896-6273(00)80633-9 · Cited by 283 · see citing works
Self-citationTARP γ-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity
Rouach, N., Byrd, K., Petralia, R. S., Elias, G. M., Adesnik, H., Tomita, S., Karimzadegan, S., Kealey, C. P., Bredt, D. S., & Nicoll, R. A. (2005) · Nature Neuroscience · doi:10.1038/nn1551 · Cited by 280 · see citing works
β-Adrenergic Regulation of Synaptic NMDA Receptors by cAMP-Dependent Protein Kinase
Raman, I. M., Tong, G., & Jahr, C. E. (1996) · Neuron · doi:10.1016/s0896-6273(00)80059-8 · Cited by 278 · see citing works
Noradrenergic Regulation of Synaptic Plasticity in the Hippocampal CA1 Region
Katsuki, H., Izumi, Y., & Zorumski, C. F. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3013 · Cited by 244 · see citing works
Hestrin, S. (1992) · Neuron · doi:10.1016/0896-6273(92)90250-h · Cited by 234 · see citing works
Svenningsson, P., Tzavara, E. T., Witkin, J. M., Fienberg, A. A., Nomikos, G. G., & Greengard, P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052712799 · Cited by 229 · see citing works
Pathway-Specific Trafficking of Native AMPARs by In Vivo Experience
Clem, R. L., & Barth, A. L. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.019 · Cited by 217 · see citing works
Gelinas, J. N., & Nguyen, P. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4175-04.2005 · Cited by 205 · see citing works
Emotional tagging of memory formation—in the search for neural mechanisms
Richter‐Levin, G., & Akirav, I. (2003) · Brain Research Reviews · doi:10.1016/j.brainresrev.2003.08.005 · Cited by 194 · see citing works
Wang, W., Zhu, W., Wang, S., Yang, D., Crow, M. T., Xiao, R.-P., & Cheng, H. (2004) · Circulation Research · doi:10.1161/01.res.0000145361.50017.aa · Cited by 192 · see citing works
State-dependent Ras signaling and AMPA receptor traffickingPreprint
Qin, Y., Zhu, Y., Baumgart, J. P., Stornetta, R. L., Seidenman, K. J., Mack, V., Aelst, L. V., & Zhu, J. (2005) · Genes & Development · doi:10.1101/gad.342205 · Cited by 177 · see citing works
Norepinephrine decreases synaptic inhibition in the rat hippocampus
Madison, D. V., & Nicoll, R. A. (1988) · Brain Research · doi:10.1016/0006-8993(88)91440-0 · Cited by 167 · see citing works
Consolidation of CS and US representations in associative fear conditioning
Frankland, P., Josselyn, S., Anagnostaras, S., Kogan, J., Takahashi, E., & Silva, A. J. (2004) · Hippocampus · doi:10.1002/hipo.10208 · Cited by 158 · see citing works
Watabe, A. M., Zaki, P. A., & O’Dell, T. J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-05924.2000 · Cited by 147 · see citing works
Long-term potentiation: studies in the hippocampal slice
Sarvey, J. M., Burgard, E. C., & Decker, G. (1989) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(89)90016-2 · Cited by 117 · see citing works
Price, C. J., Kim, P., & Raymond, L. A. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0732441.x · Cited by 109 · see citing works
Chao, S. Z., Lu, W., Lee, H., Huganir, R. L., & Wolf, M. E. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00877.x · Cited by 99 · see citing works
Self-citationGlutamatergic Plasticity by Synaptic Delivery of GluR-Blong-Containing AMPA Receptors
Kolleker, A., Zhu, J., Schupp, B. J., Qin, Y., Mack, V., Borchardt, T., Köhr, G., Malinow, R., Seeburg, P. H., & Osten, P. (2003) · Neuron · doi:10.1016/s0896-6273(03)00722-0 · Cited by 97 · see citing works
Self-citationHayley, S. P., Borowski, T. B., Merali, Z., & Anisman, H. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03262-5 · Cited by 90 · see citing works
Molecular, Cellular, and Neuroanatomical Substrates of Place Learning
Silva, A. J., Giese, K.-P., Fedorov, N. B., Frankland, P. W., & Kogan, J. H. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3837 · Cited by 90 · see citing works
AMPA receptor trafficking and synaptic plasticity: major unanswered questions.
Sheng, M., & Hyoung Lee, S. (2003) · Neuroscience Research · doi:10.1016/s0168-0102(03)00040-3 · Cited by 71 · see citing works
Vanhoose, A. M., & Winder, D. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05827.2003 · Cited by 68 · see citing works
β-Adrenergic receptors and their interacting proteins
Hall, R. A. (2004) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2003.12.017 · Cited by 67 · see citing works
A robust automated method to analyze rodent motion during fear conditioning
Kopec, C. D., Kessels, H. W. H. G., Bush, D. E. A., Cain, C. K., LeDoux, J. E., & Malinow, R. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.028 · Cited by 39 · see citing works
Self-citationHuang, C., Tsai, J.-J., & Gean, P.-W. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90295-v · Cited by 31 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Stress signalling pathways that impair prefrontal cortex structure and function
Arnsten, A. F. T. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2648 · Cited by 3,299 · see citing works
The molecular neurobiology of depression
Krishnan, V., & Nestler, E. J. (2008) · Nature · doi:10.1038/nature07455 · Cited by 2,889 · see citing works
Tononi, G., & Cirelli, C. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.025 · Cited by 2,356 · see citing works
Molecular mechanisms of fear learning and memory
Johansen, J. P., Cain, C. K., Ostroff, L. E., & LeDoux, J. E. (2011) · Cell · doi:10.1016/j.cell.2011.10.009 · Cited by 1,012 · see citing works
Self-citationAMPARs and Synaptic Plasticity: The Last 25 Years
Huganir, R. L., & Nicoll, R. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.025 · Cited by 968 · see citing works
Self-citationSynaptic AMPA receptor plasticity and behavior
Kessels, H. W., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.015 · Cited by 993 · see citing works
Self-citationExtinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories
Monfils, M.-H., Cowansage, K. K., Klann, E., & LeDoux, J. E. (2009) · Science · doi:10.1126/science.1167975 · Cited by 960 · see citing works
Self-citationThe AMPA Receptor Code of Synaptic Plasticity
Diering, G. H., & Huganir, R. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.018 · Cited by 844 · see citing works
Self-citationVyazovskiy, V. V., Cirelli, C., Pfister-Genskow, M., Faraguna, U., & Tononi, G. (2008) · Nature Neuroscience · doi:10.1038/nn2035 · Cited by 837 · see citing works
A simple role for BDNF in learning and memory?
Cunha, C. (2010) · Frontiers in Molecular Neuroscience · doi:10.3389/neuro.02.001.2010 · Cited by 778 · see citing works
Barth, C., Villringer, A., & Sacher, J. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00037 · Cited by 731 · see citing works
Ziemann, U., Reis, J., Schwenkreis, P., Rosanova, M., Strafella, A. P., Badawy, R. A. B., & Müller‐Dahlhaus, F. (2014) · Clinical Neurophysiology · doi:10.1016/j.clinph.2014.08.028 · Cited by 678 · see citing works
Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity
Yashiro, K., & Philpot, B. D. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.046 · Cited by 649 · see citing works
Han, X., Chen, M., Wang, F., Windrem, M., Wang, S., Shanz, S., Xu, Q., Oberheim, N. A., Bekar, L., Betstadt, S., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2012.12.015 · Cited by 635 · see citing works
The Hippocampal Formation in Schizophrenia
Tamminga, C. A., Stan, A. D., & Wagner, A. D. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2010.09081187 · Cited by 583 · see citing works
The Influence of Stress Hormones on Fear Circuitry
Rodrigues, S. M., LeDoux, J. E., & Sapolsky, R. M. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135620 · Cited by 556 · see citing works
Self-citationO’Donnell, J., Zeppenfeld, D. M., McConnell, E., Pena, S., & Nedergaard, M. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0818-x · Cited by 373 · see citing works
Stress and emotional memory: a matter of timing
Joëls, M., Fernández, G., & Roozendaal, B. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.04.004 · Cited by 372 · see citing works
Bornemann, B., Herbert, B. M., Mehling, W. E., & Singer, T. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01504 · Cited by 349 · see citing works
“This makes sense, as all practice-induced changes tend to be stronger, when the practice is embraced with emotional inclination and verve (Pekrun et al., 2002; Hu et al., 2007).”
GSK-3 and tau: a key duet in Alzheimer’s disease
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The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation
Groc, L., Choquet, D., & Chaouloff, F. (2008) · Nature Neuroscience · doi:10.1038/nn.2150 · Cited by 280 · see citing works
Mueller, D., Porter, J. T., & Quirk, G. J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3248-07.2008 · Cited by 284 · see citing works
Emotional enhancement of memory: how norepinephrine enables synaptic plasticity
Tully, K., & Bolshakov, V. Y. (2010) · Molecular Brain · doi:10.1186/1756-6606-3-15 · Cited by 278 · see citing works
AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine
Wolf, M. E., & Ferrario, C. R. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.01.013 · Cited by 271 · see citing works
Bocchio, M., Nabavi, S., & Capogna, M. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.022 · Cited by 260 · see citing works
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Martins, A. R. O., & Froemke, R. C. (2015) · Nature Neuroscience · doi:10.1038/nn.4090 · Cited by 233 · see citing works
Lee, H.-K., Takamiya, K., He, K., Song, L., & Huganir, R. L. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00835.2009 · Cited by 261 · see citing works
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Roelfsema, P. R., & Holtmaat, A. J. D. G. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2018.6 · Cited by 245 · see citing works
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Brzosko, Z., Mierau, S. B., & Paulsen, O. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.041 · Cited by 247 · see citing works
Glucocorticoid receptors recruit the CaMKIIα-BDNF-CREB pathways to mediate memory consolidation
Chen, D. Y., Bambah-Mukku, D., Pollonini, G., & Alberini, C. M. (2012) · Nature Neuroscience · doi:10.1038/nn.3266 · Cited by 224 · see citing works
Compartmentalized versus Global Synaptic Plasticity on Dendrites Controlled by Experience
Makino, H., & Malinow, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.036 · Cited by 219 · see citing works
Self-citationMakkar, S., Zhang, S., & Cranney, J. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.53 · Cited by 232 · see citing works
Interacting Brain Systems Modulate Memory Consolidation
McIntyre, C. K., McGaugh, J. D., & Williams, C. (2011) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.11.001 · Cited by 233 · see citing works
Genome-Wide Methylation Changes in the Brains of Suicide Completers
Labonté, B., Suderman, M., Maussion, G., Lopez, J. P., Navarro-Sánchez, L., Yerko, V., Mechawar, N., Szyf, M., Meaney, M. J., & Turecki, G. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2012.12050627 · Cited by 212 · see citing works
Sanderson, J. L., Gorski, J. A., & Dell’Acqua, M. L. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.043 · Cited by 210 · see citing works
Nitsche, M. A., Müller‐Dahlhaus, F., Paulus, W., & Ziemann, U. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.232975 · Cited by 199 · see citing works
Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory
Krugers, H. J., Hoogenraad, C. C., & Groc, L. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2913 · Cited by 197 · see citing works
Posttranslational regulation of AMPA receptor trafficking and function
Lü, W., & Roche, K. W. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.09.008 · Cited by 197 · see citing works
Xing, B., Li, Y.-C., & Gao, W.-J. (2016) · Brain Research · doi:10.1016/j.brainres.2016.01.005 · Cited by 196 · see citing works
Ritchey, M., Dolcos, F., & Cabeza, R. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm262 · Cited by 216 · see citing works
Ebitz, R. B., & Platt, M. L. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.053 · Cited by 187 · see citing works
A three-step model for the synaptic recruitment of AMPA receptors
Opazo, P., & Choquet, D. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.08.014 · Cited by 190 · see citing works
Noradrenergic Modulation of Fear Conditioning and Extinction
Giustino, T. F., & Maren, S. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00043 · Cited by 189 · see citing works
AKAP signaling complexes in regulation of excitatory synaptic plasticity
Sanderson, J. L., & Dell'Acqua, M. L. (2011) · The Neuroscientist · doi:10.1177/1073858410384740 · Cited by 185 · see citing works
Neuromodulation of hippocampal long-term synaptic plasticity
Palacios-Filardo, J., & Mellor, J. R. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.08.009 · Cited by 184 · see citing works
The developmental stages of synaptic plasticity
Löhmann, C., & Kessels, H. W. H. G. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.235119 · Cited by 176 · see citing works
Early Alterations of AMPA Receptors Mediate Synaptic Potentiation Induced by Neonatal Seizures
Rakhade, S. N., Zhou, C., Aujla, P. K., Fishman, R. E., Sucher, N. J., & Jensen, F. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1734-08.2008 · Cited by 180 · see citing works
Hebbian and neuromodulatory mechanisms interact to trigger associative memory formation
Johansen, J. P., Díaz-Mataix, L., Hamanaka, H., Ozawa, T., Ycu, E. A., Koivumaa, J., Kumar, A., Hou, M., Deisseroth, K. A., Boyden, E. S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421304111 · Cited by 179 · see citing works
Self-citationLi, S., Jin, M., Zhang, D., Yang, T., Koeglsperger, T., Fu, H., & Selkoe, D. J. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.040 · Cited by 177 · see citing works
Anterior cingulate cortex and its input to the basolateral amygdala control innate fear response
Jhang, J., Lee, H., Kang, M. S., Lee, H.-S., Park, H., & Han, J. (2018) · Nature Communications · doi:10.1038/s41467-018-05090-y · Cited by 173 · see citing works
Self-citationMechanisms of ketamine and its metabolites as antidepressants
Hess, E. M., Riggs, L. M., Michaelides, M., & Gould, T. D. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114892 · Cited by 169 · see citing works
Hämmerer, D., Callaghan, M. F., Hopkins, A. K., Kosciessa, J. Q., Betts, M. J., Cárdenas‐Blanco, A., Kanowski, M., Weiskopf, N., Dayan, P., Dolan, R. J., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712268115 · Cited by 159 · see citing works
A cholinergic trigger drives learning-induced plasticity at hippocampal synapses
Mitsushima, D., Sano, A., & Takahashi, T. (2013) · Nature Communications · doi:10.1038/ncomms3760 · Cited by 166 · see citing works
Hu, H., Qin, Y., Bochorishvili, G., Zhu, Y., Aelst, L. V., & Zhu, J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1496-08.2008 · Cited by 165 · see citing works
Self-citationO'Dell, T. J., Connor, S. A., Guglietta, R., & Nguyen, P. V. (2015) · Learning & Memory · doi:10.1101/lm.031088.113 · Cited by 163 · see citing works
TNF-α-mediated anxiety in a mouse model of multiple sclerosis
Haji, N., Mandolesi, G., Gentile, A., Sacchetti, L., Fresegna, D., Rossi, S., Musella, A., Sepman, H., Motta, C., Studer, V., et al. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.07.010 · Cited by 161 · see citing works
Magnetic resonance imaging of the human locus coeruleus: A systematic review
Liu, K. Y., Marijatta, F., Hämmerer, D., Acosta‐Cabronero, J., Düzel, E., & Howard, R. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.10.023 · Cited by 158 · see citing works
Ras and Rap Signaling in Synaptic Plasticity and Mental Disorders
Stornetta, R. L., & Zhu, J. (2010) · The Neuroscientist · doi:10.1177/1073858410365562 · Cited by 159 · see citing works
Hagena, H., Hansen, N., & Manahan‐Vaughan, D. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv330 · Cited by 163 · see citing works
Diering, G. H., Gustina, A. S., & Huganir, R. L. (2014) · Neuron · doi:10.1016/j.neuron.2014.09.024 · Cited by 153 · see citing works
Self-citationKoon, A. C., Ashley, J., Barría, R., Dasgupta, S., Brain, R., Waddell, S., Alkema, M. J., & Budnik, V. (2010) · Nature Neuroscience · doi:10.1038/nn.2716 · Cited by 146 · see citing works
Serotonin Mediates Cross-Modal Reorganization of Cortical Circuits
Jitsuki, S., Takemoto, K., Kawasaki, T., Tada, H., Takahashi, A., Bécamel, C., Sano, A., Yuzaki, M., Zukin, R. S., Ziff, E. B., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.016 · Cited by 145 · see citing works
Revest, J., Roux, A. L., Roullot, V., Kaouane, N., Vallée, M., Kasanetz, F., Rougé‐Pont, F., Tronche, F., Desmedt, A., & Piazza, P. V. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.134 · Cited by 141 · see citing works
Floriou‐Servou, A., von Ziegler, L., Stalder, L., Sturman, O., Privitera, M., Rassi, A., Cremonesi, A., Thöny, B., & Bohacek, J. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.02.003 · Cited by 126 · see citing works
Memory recall and modifications by activating neurons with elevated CREB
Kim, J., Kwon, J.-T., Kim, H.-S., Josselyn, S. A., & Han, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3592 · Cited by 136 · see citing works
Periodic Remodeling in a Neural Circuit Governs Timing of Female Sexual Behavior
Inoue, S., Yang, R., Tantry, A., Davis, C.-H. O., Yang, T., Knoedler, J. R., Wei, Y., Adams, E. L., Thombare, S. S., Golf, S. R., et al. (2019) · Cell · doi:10.1016/j.cell.2019.10.025 · Cited by 136 · see citing works
Noradrenergic modulation of extinction learning and exposure therapy.
Mueller, D., & Cahill, S. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.025 · Cited by 129 · see citing works
Pathophysiology of Locus Ceruleus Neurons in a Mouse Model of Rett Syndrome
Taneja, P., Ogier, M., Brooks-Harris, G., Schmid, D. A., Katz, D. M., & Nelson, S. B. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3156-09.2009 · Cited by 130 · see citing works
Guo, X., Hamilton, P. J., Reish, N. J., Sweatt, J. D., Miller, C. A., & Rumbaugh, G. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.223 · Cited by 120 · see citing works
Gamo, N. J., & Arnsten, A. F. T. (2011) · Behavioral Neuroscience · doi:10.1037/a0023165 · Cited by 124 · see citing works
Hains, A. B., & Arnsten, A. F. T. (2008) · Learning & Memory · doi:10.1101/lm.921708 · Cited by 127 · see citing works
Subcellular Dynamics of Type II PKA in Neurons
Zhong, H., Sia, G.-M., Sato, T., Gray, N. W., Mao, T., Khuchua, Z. A., Huganir, R. L., & Svoboda, K. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.013 · Cited by 125 · see citing works
Self-citationSlitrk1-deficient mice display elevated anxiety-like behavior and noradrenergic abnormalities
Katayama, K., Yamada, K., Ornthanalai, V. G., Inoue, T., Ota, M., Murphy, N. P., & Aruga, J. (2010) · Molecular Psychiatry · doi:10.1038/mp.2008.97 · Cited by 127 · see citing works
Coordination of Protein Phosphorylation and Dephosphorylation in Synaptic Plasticity
Woolfrey, K. M., & Dell’Acqua, M. L. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.657262 · Cited by 118 · see citing works
Positive affect and learning: exploring the “Eureka Effect” in dogs
McGowan, R. T. S., Rehn, T., Norling, Y., & Keeling, L. J. (2013) · Animal Cognition · doi:10.1007/s10071-013-0688-x · Cited by 116 · see citing works
Stress and excitatory synapses: From health to disease
Timmermans, W., Xiong, H., Hoogenraad, C. C., & Krugers, H. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.043 · Cited by 118 · see citing works
Conboy, L., & Sandi, C. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.172 · Cited by 113 · see citing works
Murphy, J. A., Stein, I. S., Lau, C. G., Peixoto, R. T., Aman, T. K., Kaneko, N., Aromolaran, K. A., Saulnier, J. L., Popescu, G., Sabatini, B. L., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4538-13.2014 · Cited by 115 · see citing works
A kinesin signaling complex mediates the ability of GSK-3β to affect mood-associated behaviors
Du, J., Wei, Y., Liu, L., Wang, Y., Khairova, R. A., Blumenthal, R., Tragon, T. R., Hunsberger, J. G., Machado‐Vieira, R., Drevets, W. C., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913138107 · Cited by 116 · see citing works
Chen, T., Koga, K., Descalzi, G., Qiu, S., Wang, J., Zhang, L.-S., Zhang, Z.-J., He, X.-B., Qin, X., Xu, F., et al. (2014) · Molecular Pain · doi:10.1186/1744-8069-10-33 · Cited by 113 · see citing works
Self-citationFaber, E. S. L., Delaney, A., Power, J., Sedlak, P. L., Crane, J. W., & Sah, P. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1796-08.2008 · Cited by 114 · see citing works
Huang, S., Treviño, M., He, K., Ardiles, Á. O., Pasquale, R. D., Guo, Y., Palacios, A. G., Huganir, R. L., & Kirkwood, A. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.023 · Cited by 112 · see citing works
Self-citationQian, H., Patriarchi, T., Price, J. L., Matt, L., Lee, B. R., Nieves‐Cintrón, M., Buonarati, O. R., Chowdhury, D., Nanou, E., Nystoriak, M. A., et al. (2017) · Science Signaling · doi:10.1126/scisignal.aaf9659 · Cited by 114 · see citing works
Learning to monitor and regulate collective thinking processes
Borge, M., Ong, Y. S., & Rosé, C. P. (2018) · International Journal of Computer-Supported Collaborative Learning · doi:10.1007/s11412-018-9270-5 · Cited by 117 · see citing works
Cortical Synaptic AMPA Receptor Plasticity during Motor Learning
Roth, R. H., Cudmore, R. H., Tan, H. L., Hong, I., Zhang, Y., & Huganir, R. L. (2019) · Neuron · doi:10.1016/j.neuron.2019.12.005 · Cited by 103 · see citing works
Self-citationLocus coeruleus-norepinephrine: basic functions and insights into Parkinson’s disease
Bari, B. A., Chokshi, V. B., & Schmidt, K. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.270297 · Cited by 106 · see citing works
A behavioural neuroscience perspective on the aetiology and treatment of anxiety disorders
Kindt, M. (2014) · Behaviour Research and Therapy · doi:10.1016/j.brat.2014.08.012 · Cited by 103 · see citing works
Goel, A., Xu, L. W., Snyder, K. P., Song, L., Goenaga-Vazquez, Y., Megill, A., Takamiya, K., Huganir, R. L., & Lee, H.-K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018264 · Cited by 103 · see citing works
Self-citationSleep: a synchrony of cell activity‐driven small network states
Krueger, J. M., Huang, Y. H., Rector, D. M., & Buysse, D. J. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12238 · Cited by 95 · see citing works
Effects of pyrethroids on brain development and behavior: Deltamethrin
Pitzer, E. M., Williams, M. T., & Vorhees, C. V. (2021) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2021.106983 · Cited by 99 · see citing works
Roles of stargazin and phosphorylation in the control of AMPA receptor subcellular distribution
Kessels, H. W. H. G., Kopec, C. D., Klein, M. E., & Malinow, R. (2009) · Nature Neuroscience · doi:10.1038/nn.2340 · Cited by 96 · see citing works
Self-citationWang, D., Govindaiah, G., Liu, R., Arcangelis, V. D., Cox, C. L., & Xiang, Y. K. (2010) · The FASEB Journal · doi:10.1096/fj.10-156661 · Cited by 95 · see citing works
Zhang, H., Etherington, L.-A., Hafner, A., Belelli, D., Coussen, F., Delagrange, P., Chaouloff, F., Spedding, M., Lambert, J. J., Choquet, D., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.80 · Cited by 92 · see citing works
Stress in the zoo: Tracking the impact of stress on memory formation over time
Vogel, S., & Schwabe, L. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.04.027 · Cited by 92 · see citing works
AMPA receptor trafficking and learning
Keifer, J., & Zheng, Z. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07339.x · Cited by 92 · see citing works
Activity-dependent synaptic plasticity modulates the critical phase of brain development
Chaudhury, S., Sharma, V., Kumar, V., Nag, T. C., & Wadhwa, S. (2015) · Brain and Development · doi:10.1016/j.braindev.2015.10.008 · Cited by 92 · see citing works
Yao, H., Liu, Y., Zhou, B., Zhang, Z., An, N., Wang, P., Wang, L., Zhang, X., & Jiang, T. (2013) · European Journal of Radiology · doi:10.1016/j.ejrad.2013.03.019 · Cited by 91 · see citing works
Harvey, B. H., & Shahid, M. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.06.014 · Cited by 88 · see citing works
Vagus Nerve Stimulation as a Potential Therapy in Early Alzheimer’s Disease: A Review
Vargas‐Caballero, M., Warming, H., Walker, R., Holmes, C., Cruickshank, G. S., & Patel, B. (2022) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.866434 · Cited by 87 · see citing works
- Authors
- Hu, H., Real, E., Takamiya, K., Kang, M.-G., Ledoux, J., Huganir, R. L., & Malinow, R.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Howard Hughes Medical Institute (US)
- New York University (US)
- Corresponding author
- Malinow, Roberto
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2007-10
- Volume
- 131
- Issue
- 1
- Pages
- 160-173
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2102170165
- Cited by
- 496
- References
- 75
- Citations by year
- 2026: 6 · 2025: 16 · 2024: 14 · 2023: 22 · 2022: 26 · 2021: 21 · 2020: 21 · 2019: 35 · 2018: 35 · 2017: 26 · 2016: 24 · 2015: 29 · 2014: 37 · 2013: 32 · 2012: 38
- FWCI
- 10.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2152 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH049159)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- norepinephrine, GluR1, AMPA receptor trafficking, GluR1 phosphorylation, long-term potentiation, emotional memory, contextual memory, emotional stress, learning and memory, neuromodulation
- MeSH terms
- Adrenergic alpha-Agonists, Animals, Behavior, Animal, Emotions, Hippocampus, Learning, Male, Memory, Mice, Transgenic, Synaptic Transmission, Norepinephrine, Synapses, Long-Term Potentiation, Receptors, AMPA, Patch-Clamp Techniques, Mice, Rats
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