Dopamine controls persistence of long-term memory storage
Abstract
The paradigmatic feature of long-term memory (LTM) is its persistence. However, little is known about the mechanisms that make some LTMs last longer than others. In rats, a long-lasting fear LTM vanished rapidly when the D1 dopamine receptor antagonist SCH23390 was injected into the dorsal hippocampus 12 hours, but not immediately or 9 hours, after the fearful experience. Conversely, intrahippocampal application of the D1 agonist SK38393 at the same critical post-training time converted a rapidly decaying fear LTM into a persistent one. This effect was mediated by brain-derived neurotrophic factor and regulated by the ventral tegmental area (VTA). Thus, the persistence of LTM depends on activation of VTA/hippocampus dopaminergic connections and can be specifically modulated by manipulating this system at definite post-learning time points.
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VTA-DA neurons play a central role in governing processes related to learning and the formation of memories associated with hedonic and motivational rewards.
“VTA-DA neurons play a central role in governing processes related to learning and the formation of memories associated with hedonic and motivational rewards (Rossato et al., 2009; Salamone and Correa, 2012; Wise, 2004).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Rossato et al., 2009
Dopaminergic neurotransmission in the hippocampus during specific time points in the retention interval is important for successful consolidation of long-term memories.
“Dopaminergic neurotransmission in the hippocampus during specific time points in the retention interval also seem to be important for successful consolidation of long-term memories (Rossato et al., 2009).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Rossato et al., 2009
DA can influence the persistence of aversive learning.
“studies also have indicated that DA can influence the persistence of aversive learning (Moncada et al., 2011; Ortiz et al., 2010; Rossato et al., 2009).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Rossato et al., 2009
A D1-like antagonist applied after training did not affect memory consolidation.
“a D1-like antagonist applied after training did not affect memory consolidation (Rossato et al., 2009).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Rossato et al., 2009
Dopamine antagonists given only during consolidation disrupt memory measured many hours later.
“Dopamine antagonists given only during such consolidation disrupt memory measured many hours later [144, 145].”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [144]
Cites
Dopamine, learning and motivation.
Wise, R. A. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1406 · Cited by 3,379 · see citing works
The hippocampal-VTA loop: controlling the entry of information into long-term memory
Lisman, J. E., & Grace, A. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.002 · Cited by 1,983 · see citing works
Bekinschtein, P., Cammarota, M., Igaz, L. M., Bevilaqua, L. R. M., Izquierdo, I., & Medina, J. H. (2007) · Neuron · doi:10.1016/j.neuron.2006.11.025 · Cited by 633 · see citing works
Self-citationDopamine: a potential substrate for synaptic plasticity and memory mechanisms
Jay, T. M. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00085-6 · Cited by 576 · see citing works
Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty
Li, S., Cullen, W. K., Anwyl, R., & Rowan, M. J. (2003) · Nature Neuroscience · doi:10.1038/nn1049 · Cited by 568 · see citing works
Huang, Y.-Y., & Kandel, E. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2446 · Cited by 544 · see citing works
Choosing the greater of two goods: neural currencies for valuation and decision making
Sugrue, L. P., Corrado, G. S., & Newsome, W. T. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1666 · Cited by 536 · see citing works
Lemon, N., & Manahan‐Vaughan, D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1454-06.2006 · Cited by 345 · see citing works
Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence
Eckel‐Mahan, K. L., Phan, T., Han, S., Wang, H., Chan, G. C. ‐., Scheiner, Z. S., & Storm, D. R. (2008) · Nature Neuroscience · doi:10.1038/nn.2174 · Cited by 344 · see citing works
Chergui, K., Charléty, P. J., Akaoka, H., Saunier, C. F., Brunet, J.-L., Buda, M., Svensson, T. H., & Chouvet, G. (1993) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1993.tb00479.x · Cited by 343 · see citing works
Frey, U., Schroeder, H., & Matthies, H. (1990) · Brain Research · doi:10.1016/0006-8993(90)91578-5 · Cited by 333 · see citing works
Dahan, L., Astier, B., Vautrelle, N., Urbain, N., Kocsis, B., & Chouvet, G. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301251 · Cited by 289 · see citing works
JOH, T. H., Park, D. H., & Reis, D. J. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.10.4744 · Cited by 284 · see citing works
Mechanism and Time Course of Cocaine-Induced Long-Term Potentiation in the Ventral Tegmental Area
Argilli, E., Sibley, D. R., Malenka, R. C., England, P. M., & Bonci, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1001-08.2008 · Cited by 243 · see citing works
Glutamate Receptors on Dopamine Neurons Control the Persistence of Cocaine Seeking
Engblom, D., Bilbao, A., Sanchis‐Segura, C., Dahan, L., Perreau‐Lenz, S., Balland, B., Parkitna, J. M. R., Luján, R., Halbout, B., Mameli, M., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.010 · Cited by 241 · see citing works
Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memoryPreprint
O’Carroll, C., Martin, S. J., Sandin, J., Frenguelli, B. G., & Morris, R. G. M. (2006) · Learning & Memory · doi:10.1101/lm.321006 · Cited by 237 · see citing works
Carter, D. A., & Fibiger, H. C. (1977) · Neuroscience · doi:10.1016/0306-4522(77)90052-5 · Cited by 181 · see citing works
Navakkode, S., Sajikumar, S., & Frey, J. U. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.02.010 · Cited by 149 · see citing works
Küppers, E., & Beyer, C. (2001) · Neuroreport · doi:10.1097/00001756-200105080-00025 · Cited by 101 · see citing works
Huang, Y.-Y., & Kandel, E. R. (2006) · Learning & Memory · doi:10.1101/lm.166906 · Cited by 47 · see citing works
Mereu, G., Lilliu, V., Casula, A., Vargiu, P., Diana, M., Musa, A., & Gessa, G. L. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00474-5 · Cited by 42 · see citing works
Gifkins, A., Greba, Q., & Kokkinidis, L. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.5.785 · Cited by 31 · see citing works
Confused about NMDA and Addiction? Targeted Knockouts Provide Answers and New Questions
Carr, D. B., & Kalivas, P. W. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.025 · Cited by 10 · see citing works
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Cited by
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Nobili, A., Latagliata, E. C., Viscomi, M. T., Cavallucci, V., Cutuli, D., Giacovazzo, G., Krashia, P., Rizzo, F. R., Marino, R., Federici, M., et al. (2017) · Nature Communications · doi:10.1038/ncomms14727 · Cited by 514 · see citing works
A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP
Lisman, J., Grace, A. A., & Duzel, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.07.006 · Cited by 465 · see citing works
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Abe, M., Schambra, H., Wassermann, E. M., Luckenbaugh, D., Schweighofer, N., & Cohen, L. G. (2011) · Current Biology · doi:10.1016/j.cub.2011.02.030 · Cited by 313 · see citing works
Plastic modifications induced by object recognition memory processing
Clarke, J. R., Cammarota, M., Gruart, A., Izquierdo, I., & Delgado-García, J. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0915059107 · Cited by 273 · see citing works
Self-citationBethus, I., Tse, D., & Morris, R. G. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2721-09.2010 · Cited by 270 · see citing works
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Lin, Q., Wei, W., Coelho, C. M., Li, X., Baker-Andresen, D., Dudley, K., Ratnu, V. S., Boskovic, Z., Kobor, M. S., Sun, Y. E., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2891 · Cited by 200 · see citing works
Memory trace replay: The shaping of memory consolidation by neuromodulation
Atherton, L. A., Dupret, D., & Mellor, J. R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.07.004 · Cited by 180 · see citing works
Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic drive
Rosen, Z. B., Cheung, S., & Siegelbaum, S. A. (2015) · Nature Neuroscience · doi:10.1038/nn.4152 · Cited by 183 · see citing works
Broussard, J. I., Yang, K., Levine, A. T., Tsetsenis, T., Jenson, D., Cao, F., Garcia, I., Arenkiel, B. R., Zhou, F.-M., De Biasi, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.070 · Cited by 180 · see citing works
“Dopaminergic neurotransmission in the hippocampus during specific time points in the retention interval also seems to be important for successful consolidation of long-term memories (Rossato et al., 2009).”
BackgroundInfluentialOrtiz, O., Delgado-García, J. M., Espadas, I., Bahí, A., Trullas, R., Dreyer, J.-L., Gruart, A., & Moratalla, R. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2655-10.2010 · Cited by 143 · see citing works
Hippocampal dopamine/DRD1 signaling dependent on the ghrelin receptor
Kern, A., Mavrikaki, M., Ullrich, C., Albarran-Zeckler, R., Brantley, A. F., & Smith, R. G. (2015) · Cell · doi:10.1016/j.cell.2015.10.062 · Cited by 136 · see citing works
Memory consolidation as an adaptive process
Cowan, E. T., Schapiro, A. C., Dunsmoor, J. E., & Murty, V. P. (2021) · Psychonomic Bulletin & Review · doi:10.3758/s13423-021-01978-x · Cited by 133 · see citing works
Sutalangka, C., Wattanathorn, J., Muchimapura, S., & Thukham-mee, W. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/695936 · Cited by 131 · see citing works
Transcranial direct-current stimulation increases extracellular dopamine levels in the rat striatum
Tanaka, T., Takano, Y., Tanaka, S., Hironaka, N., Kobayashi, K., Hanakawa, T., Watanabe, K., & Honda, M. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00006 · Cited by 125 · see citing works
“…in the modulation of motor and cognitive symptoms caused by neurological disorders such as Parkinson’s disease (PD) (Carlsson, 1972; Fahn, 2003), as well as in learning-induced neuroplasticity in both humans and rats (Adcock et al., 2006; Berridge, 2007; Rossato et al., 2009; Tanaka et al., 2011b).”
BackgroundGuzmán-Ramos, K., Moreno-Castilla, P., Castro-Cruz, M., McGaugh, J. L., Martínez-Coria, H., LaFerla, F. M., & Bermúdez-Rattoni, F. (2012) · Learning & Memory · doi:10.1101/lm.026070.112 · Cited by 127 · see citing works
Locus Coeruleus and Dopamine-Dependent Memory Consolidation
Yamasaki, M., & Takeuchi, T. (2017) · Neural Plasticity · doi:10.1155/2017/8602690 · Cited by 91 · see citing works
La Barbera, L., Vedele, F., Nobili, A., Krashia, P., Spoleti, E., Latagliata, E. C., Cutuli, D., Cauzzi, E., Marino, R., Viscomi, M. T., et al. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102031 · Cited by 98 · see citing works
“DA release in the hippocampus promotes spatial memory, reward-associated memory, novel-object recognition and memory consolidation (Broussard et al., 2016; Kempadoo et al., 2016; Mamad et al., 2017; McNamara et al., 2014; Rosen et al., 2015; Rossato et al., 2009; Takeuchi et al., 2016).”
BackgroundSchwabe, L., Höffken, O., Tegenthoff, M., & Wolf, O. T. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3304-11.2011 · Cited by 97 · see citing works
Synapse rearrangements upon learning: from divergent–sparse connectivity to dedicated sub-circuits
Caroni, P., Chowdhury, A., & Lahr, M. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.08.011 · Cited by 85 · see citing works
Neuronal reactivation during post-learning sleep consolidates long-term memory in Drosophila
Dag, U., Lei, Z., Le, J. Q., Wong, A., Bushey, D., & Keleman, K. (2019) · eLife · doi:10.7554/elife.42786 · Cited by 83 · see citing works
Cordella, A., Krashia, P., Nobili, A., Pignataro, A., La Barbera, L., Viscomi, M. T., Valzania, A., Keller, F., Ammassari-Teule, M., Mercuri, N. B., et al. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.05.006 · Cited by 82 · see citing works
Rossato, J. I., Radiske, A., Kohler, C. A., Gonzalez, C., Bevilaqua, L. R., Medina, J. H., & Cammarota, M. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.07.012 · Cited by 75 · see citing works
Self-citationFederman, N., de la Fuente, V., Zalcman, G., Corbi, N., Onori, A., Passananti, C., & Romano, A. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4181-12.2013 · Cited by 73 · see citing works
Off-line concomitant release of dopamine and glutamate involvement in taste memory consolidation
Guzmán‐Ramos, K., Osorio‐Gómez, D., Moreno‐Castilla, P., & Bermúdez‐Rattoni, F. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06758.x · Cited by 63 · see citing works
Jenson, D., Yang, K., Acevedo-Rodriguez, A., Levine, A., Broussard, J. I., Tang, J., & Dani, J. A. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.10.029 · Cited by 52 · see citing works
Rossato, J. I., Köhler, C. A., Radiske, A., Lima, R. H., Bevilaqua, L. R. M., & Cammarota, M. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.009 · Cited by 48 · see citing works
Self-citationRappeneau, V., & Castillo Díaz, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105675 · Cited by 51 · see citing works
“VTA-DA neurons play a central role in governing processes related to learning and the formation of memories associated with hedonic and motivational rewards (Rossato et al., 2009; Salamone and Correa, 2012; Wise, 2004).”
BackgroundEvidence of VTA and LC control of protein synthesis required for the behavioral tagging process
Moncada, D. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.06.003 · Cited by 50 · see citing works
Leffa, D. T., de Souza, A., Scarabelot, V. L., Medeiros, L. F., de Oliveira, C., Grevet, E. H., Caumo, W., de Souza, D. O., Rohde, L. A. P., & Torres, I. L. S. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.11.012 · Cited by 50 · see citing works
Leung, C., & Wong, Y. (2017) · Molecules · doi:10.3390/molecules22071239 · Cited by 48 · see citing works
Balderas, I., Moreno‐Castilla, P., & Bermudez‐Rattoni, F. (2013) · Hippocampus · doi:10.1002/hipo.22143 · Cited by 46 · see citing works
Menezes, J., Souto das Neves, B.-H., Gonçalves, R., Benetti, F., & Mello-Carpes, P. B. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112468 · Cited by 46 · see citing works
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Almeida-Filho, D. G., Queiroz, C. M., & Ribeiro, S. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2886-9 · Cited by 38 · see citing works
De Bundel, D., Femenía, T., DuPont, C. M., Konradsson-Geuken, Å., Feltmann, K., Schilström, B., & Lindskog, M. (2013) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713000370 · Cited by 37 · see citing works
Dopaminergic influence over hippocampal synaptic plasticity and function
I Broussard, J. (2012) · Clinical and Experimental Pharmacology · doi:10.4172/2161-1459.1000e108 · Cited by 15 · see citing works
- Authors
- Rossato, J. I., Bevilaqua, L. R. M., Izquierdo, I., Medina, J. H., & Cammarota, M.
- Affiliations
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR)
- Universidad de Buenos Aires (AR)
- Centro de Memória, Instituto do Cérebro, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brazil.
- Venue
- Science
- Published
- 2009-08-21
- Volume
- 325
- Issue
- 5943
- Pages
- 1017-1020
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2132592261
- Cited by
- 486
- References
- 23
- Citations by year
- 2026: 10 · 2025: 26 · 2024: 35 · 2023: 33 · 2022: 18 · 2021: 31 · 2020: 22 · 2019: 16 · 2018: 31 · 2017: 29 · 2016: 31 · 2015: 31 · 2014: 27 · 2013: 39 · 2012: 37
- FWCI
- 17.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- dopamine, dopamine D1 receptor, fear memory, dorsal hippocampus, ventral tegmental area, brain-derived neurotrophic factor, memory consolidation, SCH 23390
- MeSH terms
- Animals, Benzazepines, Dopamine, Fear, Hippocampus, Male, Memory, Phosphorylation, Time Factors, Tyrosine 3-Monooxygenase, 8-Bromo Cyclic Adenosine Monophosphate, 2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Receptors, Dopamine D1, Ventral Tegmental Area, Dopamine Agonists, Dopamine Antagonists, Brain-Derived Neurotrophic Factor, Rats
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