The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
Behavioral tagging is a general mechanism of long-term memory formation
Open accessAbstract
In daily life, memories are intertwined events. Little is known about the mechanisms involved in their interactions. Using two hippocampus-dependent (spatial object recognition and contextual fear conditioning) and one hippocampus-independent (conditioned taste aversion) learning tasks, we show that in rats subjected to weak training protocols that induce solely short term memory (STM), long term memory (LTM) is promoted and formed only if training sessions took place in contingence with a novel, but not familiar, experience occurring during a critical time window around training. This process requires newly synthesized proteins induced by novelty and reveals a general mechanism of LTM formation that begins with the setting of a "learning tag" established by a weak training. These findings represent the first comprehensive set of evidences indicating the existence of a behavioral tagging process that in analogy to the synaptic tagging and capture process, need the creation of a transient, protein synthesis-independent, and input specific tag.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Citations
Cites
The Organization of Behavior; A Neuropsychological Theory.
Attneave, F., B., M., & Hebb, D. O. (1950) · The American Journal of Psychology · doi:10.2307/1418888 · Cited by 5,146
The Organization of Behavior: A Neuropsychological Theory
(1950) · JAMA · doi:10.1001/jama.1950.02910470083028 · Cited by 4,272
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483
Phosphorylated CREB binds specifically to the nuclear protein CBP
Chrivia, J. C., Kwok, R. P. S., Lamb, N., Hagiwara, M., Montminy, M. R., & Goodman, R. H. (1993) · Nature · doi:10.1038/365855a0 · Cited by 2,052
Synaptic tagging and long-term potentiation
Frey, U., & Morris, R. G. M. (1997) · Nature · doi:10.1038/385533a0 · Cited by 1,736 · cited 16×
“The results resemble the pioneering work described by Frey and Morris (6) in electrophysiological model of plasticity.”
BackgroundResultInfluentialBDNF: A key regulator for protein synthesis-dependent LTP and long-term memory?
Lü, Y., Christian, K. M., & Lu, B. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.018 · Cited by 807
Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts
Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E., & Lehmann, H. (2002) · Learning & Memory · doi:10.1101/lm.41302 · Cited by 714
Conditioned Reflexes and Neuron Organization.
(1949) · Annals of Internal Medicine · doi:10.7326/0003-4819-31-6-1133_1 · Cited by 685
BDNF is essential to promote persistence of long-term memory storage
Bekinschtein, P., Cammarota, M., Katche, C., Slipczuk, L. N., Rossato, J. I., Goldin, A. P., Izquierdo, I., & Medina, J. H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711863105 · Cited by 683
Cited by
Sorted by citations
BDNF and synaptic plasticity, cognitive function, and dysfunction
Lu, B., Nagappan, G., & Lu, Y. (2014) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-45106-5_9 · Cited by 1,043
Making memories last: the synaptic tagging and capture hypothesis
Redondo, R. L., & Morris, R. G. M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2963 · Cited by 792
“Later work by the same group established the general applicability of this novelty-induced enhancement of LTM to other tasks including object recognition memory and taste conditioning, the latter being mediated by information storage in a cortical network including the insular corte”
BackgroundHippocampo-cortical coupling mediates memory consolidation during sleep
Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., & Zugaro, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4304 · Cited by 667
The synaptic plasticity and memory hypothesis: encoding, storage and persistence
Takeuchi, T., Duszkiewicz, A. J., & Morris, R. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0288 · Cited by 712
“Complementary results have been obtained using different learning tasks including taste memory, spatial object recognition, contextual fear conditioning and spatial memory [37,143,144].”
ResultMinatohara, K., Akiyoshi, M., & Okuno, H. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00078 · Cited by 535
“Arc may also be involved in a specific type of memory facilitating process called “behavioral tagging” (Moncada and Viola, 2007; Ballarini et al., 2009; Wang et al., 2010; Moncada et al., 2011).”
BackgroundA 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
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453
The Dendritic Branch Is the Preferred Integrative Unit for Protein Synthesis-Dependent LTP
Govindarajan, A., Israely, I., Huang, S.-Y., & Tonegawa, S. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.008 · Cited by 349
“Indeed, recent studies have reported behavioral data that are consistent with the STC hypothesis (Ballarini et al., 2009; Moncada and Viola, 2007).”
ResultDunsmoor, J. E., Niv, Y., Daw, N., & Phelps, E. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.028 · Cited by 329
Immediate Early Genes, Memory and Psychiatric Disorders: Focus on c-Fos, Egr1 and Arc
Gallo, F. T., Katche, C., Morici, J. F., Medina, J. H., & Weisstaub, N. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00079 · Cited by 363
“Arc also facilitates the consolidation of weak memories, and has been reported to play a role in behavioral tagging in the hippocampus (Moncada and Viola, 2007; Ballarini et al., 2009; Wang et al., 2010; Moncada et al., 2011; Martínez et al., 2012).”
BackgroundLong-term potentiation and long-term depression: a clinical perspective
Bliss, T. V. P., & Cooke, S. F. (2011) · Clinics · doi:10.1590/s1807-59322011001300002 · Cited by 333
Emotional learning selectively and retroactively strengthens memories for related events
Dunsmoor, J. E., Murty, V. P., Davachi, L., & Phelps, E. A. (2015) · Nature · doi:10.1038/nature14106 · Cited by 332
Synaptic tagging during memory allocation
Rogerson, T., Cai, D. J., Frank, A. C., Sano, Y., Shobe, J. L., López‐Aranda, M. F., & Silva, A. J. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3667 · Cited by 317
Novelty and Dopaminergic Modulation of Memory Persistence: A Tale of Two Systems
Duszkiewicz, A. J., McNamara, C. G., Takeuchi, T., & Genzel, L. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.10.002 · Cited by 324
“This physiological phenomenon can be demonstrated on a behavioural level through an analogous phenomenon of ‘behavioural tagging’ [10,12,28,66].”
Regulation and function of immediate-early genes in the brain: Beyond neuronal activity markers
Okuno, H. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.12.007 · Cited by 294
Düzel, E., Bunzeck, N., Guitart-Masip, M., & Düzel, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.08.006 · Cited by 249
Learning by the Dendritic Prediction of Somatic Spiking
Urbanczik, R., & Senn, W. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.030 · Cited by 230
“Instead, newly induced changes to synaptic strength are labile for a time frame of hours and whether they become persistent can even depend on seemingly unrelated behavioral events (Ballarini et al., 2009).”
Wang, S.-H., Redondo, R. L., & Morris, R. G. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008638107 · Cited by 251
An opportunistic theory of cellular and systems consolidation
Mednick, S. C., Cai, D. J., Shuman, T., Anagnostaras, S., & Wixted, J. T. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.003 · Cited by 267
Interacting brain systems modulate memory consolidation
McIntyre, C. K., McGaugh, J. L., & Williams, C. L. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.11.001 · Cited by 243
“This effect depends upon protein synthesis at the time of exposure to the novel stimulus (Ballarini et al., 2009).”
BackgroundEmerging roles of metaplasticity in behaviour and disease
Hulme, S. R., Jones, O. D., & Abraham, W. C. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.03.007 · Cited by 209
Synaptic clustering within dendrites: An emerging theory of memory formation
Kastellakis, G., Cai, D. J., Mednick, S. C., Silva, A. J., & Poirazi, P. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.12.002 · Cited by 198
“…normally induces short-term memory, with environmental novelty, it was found that novelty – considered a strong learning event – promotes the formation of long-term memory, presumably through the mechanisms of STC (Ballarini et al., 2009; De Carvalho Myskiw et al., 2013; Moncada and Viola, 2007).”
Influence of reward motivation on human declarative memory
Lombard, E., Bavelier, D., & Schwartz, S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.11.015 · Cited by 191
Moncada, D., Ballarini, F., Martinez, M. C., Frey, J. U., & Viola, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104495108 · Cited by 171
“Based on the synaptic tagging and capture hypothesis (7, 8), we recently proposed that the formation of different LTMs depends on two stages: an initial stage consisting of the tagging of specific sites where the information is encoded and a later stage during which PRPs are captured at those tagged sites (1, 2).”
BackgroundReset of hippocampal–prefrontal circuitry facilitates learning
Park, A. J., Harris, A. Z., Martyniuk, K. M., Chang, C., Abbas, A. I., Lowes, D. C., Kellendonk, C., Gogos, J. A., & Gordon, J. A. (2021) · Nature · doi:10.1038/s41586-021-03272-1 · Cited by 153
“f, Learning curve (logistic regression model; F(39,1365) = 2.”
Long‐term plasticity in the hippocampus: maintaining within and ‘tagging’ between synapses
Bin Ibrahim, M. Z., Benoy, A., & Sajikumar, S. (2022) · The FEBS Journal · doi:10.1111/febs.16065 · Cited by 137
Behavioral Tagging: A Translation of the Synaptic Tagging and Capture Hypothesis
Moncada, D., Ballarini, F., & Viola, H. (2015) · Neural Plasticity · doi:10.1155/2015/650780 · Cited by 137
“Rats that received a low dose of LiCl (weak training) induced a negligible CTA-LTM but expressed a strong CTASTM measured 30 minutes after the acquisition session [53].”
BackgroundResultInfluentialMemory 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
The learning of fear extinction
Furini, C., Myskiw, J., & Izquierdo, I. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.016 · Cited by 124
Behavioral tagging of extinction learning
Myskiw, J. D. C., Benetti, F., & Izquierdo, I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220875110 · Cited by 126
“Novelty, as used here and in related experiments on behavioral tagging, refers to exposure to an open field (OF) (15, 18, 19) or a holeboard (12), the exploration of which causes habituation learning and engenders hippocampal biochemical changes (42–44) that usually lead to protein synthesis.”
BackgroundMethodResultInfluentialDopaminergic innervation and modulation of hippocampal networks
Edelmann, E., & Leßmann, V. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2800-7 · Cited by 117
“…be relevant for the formation of hippocampus-dependent long-term memory (LTM) induced by so-called behavioral tagging (e.g., Moncada and Viola 2007; Ballarini et al. 2009; Rogerson et al. 2014; Moncada et al. 2015; Nomoto et al. 2016; Vishnoi et al. 2016; Moncada 2017), where a weak training…”
BackgroundKastellakis, G., Silva, A. J., & Poirazi, P. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.015 · Cited by 107
Locus Coeruleus and Dopamine-Dependent Memory Consolidation
Yamasaki, M., & Takeuchi, T. (2017) · Neural Plasticity · doi:10.1155/2017/8602690 · Cited by 91
Memory in Elementary School Children Is Improved by an Unrelated Novel Experience
Ballarini, F., Martínez, M. C., Perez, M. D., Moncada, D., & Viola, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066875 · Cited by 107
“In this regard, previous work in rodents has demonstrated that a novel behavioral experience can promote the formation of a long-lasting memory for another task when novelty occurs within a restricted time window around the learning task [11,12,13,14,15].”
BackgroundCellular tagging as a neural network mechanism for behavioural tagging
Nomoto, M., Ohkawa, N., Nishizono, H., Yokose, J., Suzuki, A. Z., Matsuo, M., Tsujimura, S., Takahashi, Y., Nagase, M., Watabe, A. M., et al. (2016) · Nature Communications · doi:10.1038/ncomms12319 · Cited by 93
Emotional tagging—A simple hypothesis in a complex reality
Bergado, J. A., Lucas, M., & Richter‐Levin, G. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.03.004 · Cited by 98
Dong, Z., Gong, B., Li, H., Bai, Y., Wu, X., Huang, Y. Y., He, W., Li, T., & Wang, Y. T. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0984-12.2012 · Cited by 89
“In addition, recent studies also proposed that novelty exploration may promote LTM formation through the mechanism of behavioral tagging and capture processes (Moncada and Viola, 2007; Ballarini et al., 2009).”
BackgroundA predictive account of how novelty influences declarative memory
Quent, J. A., Henson, R. N., & Greve, A. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107382 · Cited by 84
“, from novelty) has to be experienced to cause long-lasting memory change (Ballarini et al., 2009; Moncada & Viola, 2007).”
Myskiw, J. D. C., Furini, C. R. G., Benetti, F., & Izquierdo, I. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400423111 · Cited by 81
“Because many learned behaviors rely on hippocampal LTP or LTD (7–9), among them the processing of novelty (9, 10) and the making of extinction (11–13), interactions between consecutive learnings can also be explained by the “tagging-and-capture” hypothesis (9, 10, 13), whose application to behavior became known as “be…”
BackgroundMethodSchumacher, A., Vlassov, E., & Ito, R. (2015) · Hippocampus · doi:10.1002/hipo.22542 · Cited by 76
“Such an account would also be difficult to reconcile with substantial data, which implicate the dorsal HPC preferentially in novelty processing (Lisman and Grace 2005; Moncada and Viola 2007; Honey et al., 2008; Hunsaker et al., 2008; Ballarini et al., 2009; Wells et al., 2013).”
ResultSynaptic tagging and capture in the living rat
Shires, K. L., Silva, B. M. D., Hawthorne, J. P., Morris, R., & Martin, S. J. (2012) · Nature Communications · doi:10.1038/ncomms2250 · Cited by 72
Initial memory consolidation and the synaptic tagging and capture hypothesis
Okuda, K., Højgaard, K., Privitera, L., Bayraktar, G., & Takeuchi, T. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14902 · Cited by 74
“Infusion of the protein synthesis inhibitor anisomycin before or immediately after novelty has been shown to impair consolidation of a transient weak memory into LTM (Moncada & Viola, 2007; Ballarini et al., 2009; Wang et al., 2010).”
BackgroundInfluentialHippocampal ripples as a mode of communication with cortical and subcortical areas
Todorova, R., & Zugaro, M. (2018) · Hippocampus · doi:10.1002/hipo.22997 · Cited by 77
“In order to determine whether this could potentially improve memory consolidation, they used a modified version (Ballarini et al., 2009) of a classical spatial memory task: rats were first placed in a rectangular arena with two identical objects in adjacent corners (sampling); on the following day…”
MethodTag and capture: how salient experiences target and rescue nearby events in memory
Dunsmoor, J. E., Murty, V. P., Clewett, D., Phelps, E. A., & Davachi, L. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.06.009 · Cited by 84
Dockery, C. A., Liebetanz, D., Birbaumer, N., Malinowska, M., & Wesierska, M. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.06.018 · Cited by 76
Menezes, J., Alves, N., Borges, S., Roehrs, R., Myskiw, J. D. C., Furini, C. R. G., Izquierdo, I., & Mello‐Carpes, P. B. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1502295112 · Cited by 76
“The control group was not exposed to novelty, whereas the groups exposed to novelty 30 min before the first extinction training session received bilateral intrahippocampal infusion of vehicle (VEH) or of the protein synthesis inhibitor ANI (80 μg/μL–1 μL per side) immediately after the exposure to OF.”
BackgroundMethodInfluentialAlmaguer‐Melian, W., Bergado, J. A., Fuentes, N. P., Alberti‐Amador, E., Mercerón‐Martínez, D., & Frey, J. U. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114198109 · Cited by 71
Clayton, D. F., Anreiter, I., Aristizabal, M. J., Frankland, P. W., Binder, E. B., & Citri, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820837116 · Cited by 67
Synaptic consolidation: an approach to long-term learning
Clopath, C. (2011) · Cognitive Neurodynamics · doi:10.1007/s11571-011-9177-6 · Cited by 77
“E stands for the energy landscape of the late-weight, showing the two stable states unless the tag and the plasticity-related proteins are presents, then E only has one stable state. d–f Consolidation Model by Barrett et al. (2009).”
BackgroundResultInfluentialEvent segmentation protects emotional memories from competing experiences encoded close in time
Dunsmoor, J. E., Kroes, M. C. W., Moscatelli, C. M., Evans, M. D., Davachi, L., & Phelps, E. A. (2018) · Nature Human Behaviour · doi:10.1038/s41562-018-0317-4 · Cited by 77
Hypothesized mechanisms through which acute exercise influences episodic memory
Loprinzi, P. D., Ponce, P., & Frith, E. (2018) · Physiology International · doi:10.1556/2060.105.2018.4.28 · Cited by 67
“expression from exercise; and (6) exercise enhancing dendritic spine growth.”
BackgroundLi, Q., Rothkegel, M., Xiao, Z., Abraham, W. C., Körte, M., & Sajikumar, S. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs315 · Cited by 64
Behavioral specifications of reward-associated long-term memory enhancement in humans
Wittmann, B. C., Dolan, R. J., & Düzel, E. (2011) · Learning & Memory · doi:10.1101/lm.1996811 · Cited by 62
“These studies report lasting effects of novelty on subsequent hippocampal plasticity (Li et al., 2003; Ballarini et al., 2009) and hippocampus-dependent memory for stimuli occurring within 30 minutes after exposure to novelty (Fenker et al.”
InfluentialWong, L., Tann, J. Y., Ibáñez, C. F., & Sajikumar, S. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2876-18.2019 · Cited by 63
“Our study has thus identified p75NTR as a promising target to limit the cognitive deficits associated with SD. 5452 • The Journal of Neuroscience, July 10, 2019 • 39(28):5452–5465 ronal population (Frey and Morris, 1997; Ballarini et al., 2009; Redondo and Morris, 2011).”
BackgroundThe neuroscience of active learning and direct instruction
Dubinsky, J. M., & Hamid, A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105737 · Cited by 121
“To be influenced by synaptic tagging, weakly encoded events must occur within specific time windows, roughly 0.5 – 3 hr before or after the more memorable event (Ballarini et al., 2009; Frey Box 2 Synopsis of the Neural Substrates of Human Learning and Memory.”
BackgroundInfluentialTransient Astrocytic Gq Signaling Underlies Remote Memory Enhancement
Iwai, Y., Ozawa, K., Yahagi, K., Mishima, T., Akther, S., Vo, C. T., Lee, A. B., Tanaka, M., Itohara, S., & Hirase, H. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.658343 · Cited by 57
Otmakhova, N. A., Düzel, E., Deutch, A. Y., & Lisman, J. E. (2012) · Springer eBooks · doi:10.1007/978-3-642-32375-1_10 · Cited by 59
“" Following this framework, Ballarini et al. (2009) found that the persistence of a memory induced by weak training could be enhanced by concurrent strong training in another task.”
BackgroundSharma, M., Shetty, M. S., Arumugam, T. V., & Sajikumar, S. (2015) · Scientific Reports · doi:10.1038/srep16616 · Cited by 55
Johnson, A. C., Miller, J. E., & Cipolla, M. J. (2019) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x19848510 · Cited by 60
“The acquisition phase consisted of each rat being placed in the arena with two identical objects and allowed to explore for 10min, an exposure time of sufficient duration to induce, and therefore test, long-term memory.(27) After the acquisition phase, rats were returned to their home cages.”
MethodSynaptic Consolidation: From Synapses to Behavioral Modeling
Ziegler, L., Zenke, F., Kastner, D. B., & Wulfram Gerstner, B. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3989-14.2015 · Cited by 55
“Thispredictionmaylooksur-prisinginviewoftheexistingliterature(cf.Ballarinietal.,2009vs MoncadaandViola,2007).”
BackgroundSalvetti, B., Morris, R., & Wang, S. (2014) · Learning & Memory · doi:10.1101/lm.032177.113 · Cited by 57
“…memory persistence of inhibitory avoidance (Moncada and Viola 2007; Lu et al. 2011), contextual fear conditioning and spatial object recognition (Ballarini et al. 2009), spatial memory in the event arena (Wang et al. 2010), spatial memory in the water maze (Almaguer-Melian et al. 2012), and…”
BackgroundMethodResultInfluentialThe Tagging and Capture Hypothesis from Synapse to Memory
Viola, H., Ballarini, F., Martínez, M. C., & Moncada, D. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-420170-5.00013-1 · Cited by 60
Selective Memory Generalization by Spatial Patterning of Protein Synthesis
O’Donnell, C., & B, T. J. S. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.028 · Cited by 51
“…memories for events occurring within the same environment but that it can act as a powerful mechanism for selective consolidation of hippocampal memories for events occurring in distinct environments, as observed experimentally (Ballarini et al., 2009; Moncada and Viola, 2007; Wang et al., 2010).”
Influential‘Tagging’ along memories in aging: Synaptic tagging and capture mechanisms in the aged hippocampus
Shetty, M. S., & Sajikumar, S. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.12.008 · Cited by 54
Large-Scale Fluorescence Calcium-Imaging Methods for Studies of Long-Term Memory in Behaving MammalsPreprint
Jercog, P. E., Rogerson, T., & Schnitzer, M. J. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021824 · Cited by 56
“Similarly, behavioral (Ballarini et al. 2009) and cell biological (Frey and Morris 1997) phenomena in which one set of events impacts the encoding of other temporally separated events indicate that memories are not encoded in isolation, but rather in relation to prior and subsequent events (Moncada…”
BackgroundOn the transition from reconsolidation to extinction of contextual fear memories
Cassini, L. F., Flavell, C. R., Amaral, O. B., & Lee, J. L. C. (2017) · Learning & Memory · doi:10.1101/lm.045724.117 · Cited by 47
Actin remodeling, the synaptic tag and the maintenance of synaptic plasticity
Pinho, J., Marcut, C. F., & Fonseca, R. (2020) · IUBMB Life · doi:10.1002/iub.2261 · Cited by 50
Evidence 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
“For three days animals were submitted to these recording boxes during 30 min in order to make them familiar and avoid any spatial novelty during the stimulation in the experimental day (Ballarini et al., 2009; Moncada & Viola, 2007).”
Clewett, D., Dunsmoor, J. E., Bachman, S. L., Phelps, E. A., & Davachi, L. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107572 · Cited by 49
“…While the neural processes supporting this memory benefit are unknown, one compelling neurobiological mechanism is ‘synaptic tagging ’ (Frey & Morris 1997) and its behavioral counterpart ‘behavioral tagging ’ (Ballarini et al., 2009; Moncada et al., 2011; Moncada & Viola, 2007; Wang et al., 2010).”
Modulation of the extinction of fear learning
Myskiw, J. D. C., Izquierdo, I., & Furini, C. R. G. (2014) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2014.04.006 · Cited by 44
Okuno, H., Minatohara, K., & Bito, H. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.025 · Cited by 45
Bréchet, L., Hausmann, S. B., Mange, R., Herbelin, B., Blanke, O., & Serino, A. (2020) · Brain and Behavior · doi:10.1002/brb3.1571 · Cited by 44
“…in rats how weak episodes of training, which would be forgotten, may be stored in long-term memory if then associated to a novel, salient experience, the so-called synaptic-behavioral tagging (Ballarini, Moncada, Martinez, Alen, & Viola, 2009; Moncada, Ballarini, & Viola, 2015; Wang et al., 2010).”
BackgroundLiu, J., Yang, C., Deng, J., Yan, W., Wang, H.-M., Luo, Y., Shi, H., Meng, S., Chai, B.-S., Fang, Q., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0005-15.2015 · Cited by 43
“Cyclic adenosine monophosphate response element binding protein (CREB) may also be involved in the synthesis of PRPs (Ballarini et al., 2009).”
BackgroundMethodInfluentialNovelty Improves the Formation and Persistence of Memory in a Naturalistic School Scenario
Butavand, D. R., Hirsch, I., Tomaiuolo, M., Moncada, D., Viola, H., & Ballarini, F. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.00048 · Cited by 41
Memory allocation mechanisms underlie memory linking across time
Sehgal, M., Zhou, M., Lavi, A., Huang, S., Zhou, Y., & Silva, A. J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.02.021 · Cited by 41
Bridging Synaptic and Epigenetic Maintenance Mechanisms of the Engram
Kyrke‐Smith, M., & Williams, J. M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00369 · Cited by 43
“This tagging phenomenon has also been identified in relation to memory, called instead behavioral tagging, where weak memories can become long-term memories when associated with a strong learning experience which would elicit this central gene response (Bear, 1997; Ballarini et al., 2009; Lesburguères et al., 2011; Re…”
BackgroundBehavioral tagging underlies memory reconsolidation
Orlandi, I. R., Fullio, C. L., Schroeder, M. N., Giurfa, M., Ballarini, F., & Moncada, D. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2009517117 · Cited by 44
Memory consolidation and improvement by synaptic tagging and capture in recurrent neural networks
Luboeinski, J., & Tetzlaff, C. (2021) · Communications Biology · doi:10.1038/s42003-021-01778-y · Cited by 41
Martínez, M. C., Alen, N., Ballarini, F., Moncada, D., & Viola, H. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.05.007 · Cited by 40
Medial prefrontal cortex dopamine controls the persistent storage of aversive memories
González, M. C., Kramar, C. P., Tomaiuolo, M., Katche, C., Weisstaub, N., Cammarota, M., & Medina, J. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00408 · Cited by 42
“Experiments were conducted in male Wistar rats (UBA, Argentina and UFRN, Brazil) weighting 220–250 g. Animals were housed five to a cage and kept at a constant temperature of 23◦C, with water and food ad libitum, under a 12-h light/dark cycle (lights on at 7:00 a.m.).”
MethodEmotional learning retroactively enhances item memory but distorts source attributionPreprint
Hennings, A. C., Lewis‐Peacock, J. A., & Dunsmoor, J. E. (2021) · Learning & Memory · doi:10.1101/lm.053371.120 · Cited by 46
“For example, the behavioral tagging hypothesis (derived from the synaptic tagging hypothesis; Frey and Morris 1997) proposes that weak learning is strengthened in memory if it is encoded within a critical time window of a more salient event and if the two events share overlapping neural ensembles (Moncada and Viola 20…”
BackgroundQuinlan, M. A. L., Strong, V., Skinner, D. M., Martin, G. M., Harley, C. W., & Walling, S. G. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00067 · Cited by 38
Hippocampal neurons with stable excitatory connectivity become part of neuronal representations
Castello-Waldow, T. P., Weston, G., Ulivi, A. F., Chenani, A., Loewenstein, Y., Chen, A., & Attardo, A. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000928 · Cited by 33
Cassini, L. F., Sierra, R. O., Haubrich, J., Crestani, A. P., Santana, F., de Oliveira Alvares, L., & Quillfeldt, J. A. (2013) · Hippocampus · doi:10.1002/hipo.22149 · Cited by 36
“The possibility that this protein synthesis was induced by the wSOR is negligible since Ballarini et al. (2009) have shown that inhibition of protein synthesis have no effect when administered right before the very same weak training (wSOR).”
BackgroundMethodInfluentialEngram mechanisms of memory linking and identity
Choucry, A., Nomoto, M., & Inokuchi, K. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00814-0 · Cited by 41
“Synaptic tagging and capture mechanisms can therefore explain the potentiation of weak memories that can occur when they are temporally proximate to stronger events 46,136,137 (but also see ref.”
The neuroscience of positive memory deficits in depression
Dillon, D. G. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01295 · Cited by 40
“This confirms a central prediction of STC: once PRPs are made available—here, by novelty exposure—they can be captured by tags that are set shortly afterward, even if PRP production is blocked during tag setting (see also Moncada and Viola, 2007; Ballarini et al., 2009).”
BackgroundDifferential Contribution of Hippocampal Subfields to Components of Associative Taste Learning
Adaikkan, C., Wintzer, M. E., McHugh, T. J., & Rosenblum, K. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0956-14.2014 · Cited by 34
“…learning and memory, following pharmacologically mediated inactivation or hippocampal lesions (Murphy and Brown, 1974; Miller et al., 1975, 1986; Bakner et al., 1991; Reilly et al., 1993; Purves et al., 1995; Yamamoto et al., 1995; Stone et al., 2005; De la Cruz et al., 2008; Ding et al., 2008;…”
BackgroundInfluentialBehavioral tagging: A novel model for studying long-term memory
Vishnoi, S., Raisuddin, S., & Parvez, S. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.017 · Cited by 35
Sharma, M., Razali, N. B., & Sajikumar, S. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw170 · Cited by 32
Awad, W., Ferreira, G., & Maroun, M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.103 · Cited by 35
Behavioral and neural mechanisms by which prior experience impacts subsequent learning
Parsons, R. G. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.11.008 · Cited by 35
“Weak conditioned taste aversion training can be transformed into LTM if rats were exposed to a novel taste an hour before training (Ballarini et al., 2009).”
InfluentialThe Quest for the Hippocampal Memory Engram: From Theories to Experimental Evidence
Miry, O., Li, J., & Chen, L. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.632019 · Cited by 40
“Specifically, when an animal is acquiring a weak memory of a non-salient experience, and a neuron involved in the acquisition of this memory has recently participated in the acquisition of a strong memory of a salient experience, the synapses activated during weak-memory acquisition are expected to utilize the PRPs pr…”
BackgroundFragile X mental retardation protein regulates heterosynaptic plasticity in the hippocampusPreprint
Connor, S. A., Hoeffer, C. A., Klann, E., & Nguyen, P. (2011) · Learning & Memory · doi:10.1101/lm.2043811 · Cited by 32
“likely to involve “behavioral tagging” (Moncada and Viola 2007; Ballarini et al. 2009).”
BackgroundMemory of Conditioned Taste Aversion Is Erased by Inhibition of PI3K in the Insular Cortex
Slouzkey, I., Rosenblum, K., & Maroun, M. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.20 · Cited by 30
Shetty, M. S., Gopinadhan, S., & Sajikumar, S. (2015) · Hippocampus · doi:10.1002/hipo.22497 · Cited by 31
“…tagging and capture have gained a lot of supportive evidence recently with studies demonstrating such mechanisms in anesthetized and freely moving animals, both from electrophysiological recordings and behavioral paradigms (Ballarini et al., 2009; Redondo and Morris, 2011; Shires et al., 2012).”
BackgroundBehavioral, cellular, and synaptic tagging frameworks
Nomoto, M., & Inokuchi, K. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.010 · Cited by 31
Behavioral tagging and capture: long-term memory decline in middle-aged rats
Gros, A., & Wang, S. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.02.023 · Cited by 30
Exploration of a novel virtual environment improves memory consolidation in ADHD
Baumann, V., Birnbaum, T., Breitling-Ziegler, C., Tegelbeckers, J., Dambacher, J., Edelmann, E., Bergado-Acosta, J. R., Flechtner, H., & Krauel, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-78222-4 · Cited by 33
Hippocampal NMDA receptors and the previous experience effect on memory
Cercato, M. C., Colettis, N. C., Snitcofsky, M., Aguirre, A. I., Kornisiuk, E. E., Báez, M. V., & Jerusalinsky, D. A. (2014) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2014.08.001 · Cited by 30
“…2008) generated by the previous (OF) experience, which would contribute to encoding the 2nd task (IA), leading to consolidation whenever the traces of both tasks are processed (at least partially) in the same structure (sharing some circuits) (Ballarini et al., 2009; Moncada and Viola, 2007).”
BackgroundEffects of active exploration on novelty-related declarative memory enhancement
Schomaker, J., & Wittmann, B. C. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107403 · Cited by 29
Metadata
- Authors
- Ballarini, F., Moncada, D., Martinez, M. C., Alen, N., & Viola, H.
- Affiliations
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- Instituto de Biología Celular y Neurociencias, Facultad de Medicina, Universidad de Buenos Aires-CONICET, Paraguay 2155, 3° Piso, CP 1121, Buenos Aires, Argentina; and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-08-25
- Volume
- 106
- Issue
- 34
- Pages
- 14599-14604
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2732837
- OpenAlex
- W2146205533
- Cited by
- 301
- References
- 39
- Citations by year
- 2026: 12 · 2025: 19 · 2024: 38 · 2023: 23 · 2022: 15 · 2021: 18 · 2020: 22 · 2019: 15 · 2018: 22 · 2017: 14 · 2016: 24 · 2015: 18 · 2014: 23 · 2013: 13 · 2012: 9
- FWCI
- 4.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Repositorio Digital Institucional de la Universidad de Buenos Aires (Universidad de Buenos Aires) (publishedVersion, other-oa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- long-term memory formation, synaptic tagging and capture, short-term memory, hippocampal-dependent memory, contextual fear conditioning, conditioned taste aversion, protein synthesis, memory consolidation, rats
- MeSH terms
- Animals, Behavior, Animal, Conditioning, Psychological, Discrimination Learning, Fear, Hippocampus, Learning, Male, Memory, Memory, Short-Term, Neuronal Plasticity, Psychomotor Performance, Saccharin, Sodium Chloride, Spatial Behavior, Taste, Time Factors, Rats, Wistar, Long-Term Potentiation, Neocortex, 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
