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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.
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Experimental Preeclampsia Causes Long-Lasting Hippocampal Vascular Dysfunction and Memory Impairment
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“7 , 2837 – 2843. Ballarini, F., Moncada, D., Martinez, M.C., Alen, N., and Viola, H. (2009). Behavioral tagging is a general mechanism of long-term memory formation.”
BackgroundSpatial object recognition memory formation under acute stress
da Cunha, P. L., Villar, M. E., Ballarini, F., Tintorelli, R., & Viola, H. (2018) · Hippocampus · doi:10.1002/hipo.23037 · Cited by 20
“…fear conditioning reminder session, contextual fear condi- tioning extinction session or a rewarded T-maze task were further described as protein supplier events that promote unrelated memories (Ballarini et al., 2009; Cassini et al., 2013; Dong et al., 2012; Salvetti, Morris, & Wang, 2014).”
BackgroundInfluentialNovelty enhances memory persistence and remediates propranolol-induced deficit via reconsolidation
Wang, S. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.08.015 · Cited by 20
“This principle has been shown to enable persistence of a wide range of memory types, such as contextual fear memory, conditioned taste memory, and object recognition memory (Ballarini et al., 2009).”
InfluentialNaseem, M., Tabassum, H., & Parvez, S. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.03.060 · Cited by 20
Lima, K. R., de Vargas, L. D. S., Ramborger, B. P., Roehrs, R., Sevenster, D., Izquierdo, I., D’Hooge, R., & Mello‐Carpes, P. B. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111991 · Cited by 19
Broadbelt, T., Mutlu-Smith, M., Carnicero-Senabre, D., Saido, T. C., Saito, T., & Wang, S. (2022) · Scientific Reports · doi:10.1038/s41598-022-26113-1 · Cited by 21
Tintorelli, R., Budriesi, P., Villar, M. E., Marchal, P., da Cunha, P. L., Correa, J., Giurfa, M., & Viola, H. (2020) · Scientific Reports · doi:10.1038/s41598-019-57007-4 · Cited by 19
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“…driven by reward (Braun et al., 2018; * Aya Ben-Yakov aya.ben-yakov@mrc-cbu.cam.ac.uk 1 MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK Murayama & Kitagami, 2014; Patil et al., 2017) and novelty (Ballarini et al., 2009, 2013; Fenker et al., 2008; Wang et al., 2010).”
BackgroundThe role of the gustatory cortex in incidental experience-evoked enhancement of later taste learningPreprint
Flores, V. L., Parmet, T., Mukherjee, N., Nelson, S. B., Katz, D. B., & Levitan, D. (2018) · Learning & Memory · doi:10.1101/lm.048181.118 · Cited by 20
“…has been shown to affect both neural development and specific sensory responses (Alwis and Rajan 2013; Liu and Urban 2017); and 2) “innocuous” stimuli have been suggested to enhance sub-threshold learning experiences (Ballarini et al. 2009) and latent inhibition (Merhav and Rosenblum 2008).”
BackgroundInfluentialCooper, S. E., Hennings, A. C., Bibb, S. A., Lewis‐Peacock, J. A., & Dunsmoor, J. E. (2024) · Current Biology · doi:10.1016/j.cub.2024.06.071 · Cited by 21
Effect of context exposure after fear learning on memory generalization in mice
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“sary for behavioral tagging [32], whereas it is not essential for memory generalization, as found in the present study.”
ResultSynapses tagged, memories kept: synaptic tagging and capture hypothesis in brain health and disease
Ibrahim, M. Z. B., Wang, Z., & Sajikumar, S. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0237 · Cited by 16
“Briefly, behavioural tagging occurs when a transient memory achieves memory persistence owing to the proximity of its encoding to a strong memory encoding event [10,80].”
BackgroundMethodRansome, M. I., & Hannan, A. J. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.01.004 · Cited by 17
Facilitation of responses by task-irrelevant complex deviant stimuli
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The Behavioral Tagging Hypothesis and Its Implications for Long-Term Memory Formation
Moncada, D., Ballarini, F., Martínez, M. C., & Viola, H. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1761-7_14 · Cited by 17
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“…conducted with a view to a behavioral project looking at the functional impact of STC, sometimes called “behavioral tagging” (Moncada and Viola 2007; Ballarini et al. 2009; Wang et al. 2010; Moncada et al. 2011), the focus here being to establish baseline forgetting functions for rapidly acquired…”
BackgroundGannon, O. J., Tremble, S. M., McGinn, C., Guth, R., Scoppettone, N., Hunt, R. D., Prakash, K., & Johnson, A. C. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.13491 · Cited by 15
“38 index as a measure of long-term memory function.”
BackgroundNew frontiers in the study of memory mechanisms
Furini, C. R. G., Myskiw, J. D. C., Benetti, F., & Izquierdo, I. (2013) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2012-1046 · Cited by 16
Preexposure to salty and sour taste enhances conditioned taste aversion to novel sucrosePreprint
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“Our paradigm is very different from that shown to cause behavioral tagging in a CTA context (Ballarini et al. 2009)—the delay between final preexposure and conditioning was longer in our experiments by a factor of .”
MethodCuriosity shapes spatial exploration and cognitive map formation in humans
Cen, D., Teichert, E., Hodgetts, C. J., & Gruber, M. J. (2024) · Communications Psychology · doi:10.1038/s44271-024-00174-6 · Cited by 19
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“Indeed, BTT only predicts a memory benefit for material that is processed in the same brain region in which a novel experience has triggered plasticity-related proteins (PRPs).”
BackgroundResultInfluentialA novelty-retrieval-extinction paradigm leads to persistent attenuation of remote fear memories
Huang, F., Zou, G.-J., Li, C., Meng, H., Liu, X., & Yang, Z. (2020) · Scientific Reports · doi:10.1038/s41598-020-60176-2 · Cited by 14
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“For the NOR task, each rat was allowed to habituate to the open field arena for five minutes, followed by acquisition period exploring two identical objects for 10 min (Ballarini et al., 2009).”
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“…(IA) (Menezes et al., 2015; Moncada, 2017; Moncada et al., 2011; Myskiw et al., 2013; Rabinovich et al., 2020), spatial object recognition (SOR) (Ballarini et al., 2009), novel object recognition (NOR) (Nomoto et al., 2016), appetitive (Gros & Wang, 2018) and spatial tasks (Almaguer-Melian et…”
BackgroundInfluentialA circuit mechanism linking past and future learning through shifts in perception
Crossley, M., Benjamin, P. R., Kemenes, G., Staras, K., & Kemenes, I. (2023) · Science Advances · doi:10.1126/sciadv.add3403 · Cited by 11
“This differs from a previously identified process, behavioral tagging (38, 39), which facilitates the interaction and enhancement of memories based on synaptic tag and capture (40, 41).”
BackgroundAdaptive memory systems for remembering the salient and the seemingly mundane
Ritchey, M., Murty, V. P., & Dunsmoor, J. E. (2016) · Behavioral and Brain Sciences · doi:10.1017/s0140525x15001922 · Cited by 13
Nutritional stress timing differentially programs cognitive abilities in young adult male mice
Berardino, B. G., Ballarini, F., Chertoff, M., Igaz, L. M., & Cánepa, E. T. (2020) · Nutritional Neuroscience · doi:10.1080/1028415x.2020.1751507 · Cited by 10
“To analyze the impact of the low-protein diets on aversive memory, we used the conditioned taste aversion test adapted from a previous study [30].”
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“…our study was purely behavioral and did not incorporate a long-term memory test, one model supporting memory enhancements for otherwise mundane information is known as behavioral tagging (Ballarini et al., 2009; Redondo & Morris, 2011), based on the synaptic tag-and-capture (Frey and Morris, 1997).”
Behavioral tagging as a mechanism for aversive‐memory formation under acute stress
da Cunha, P. L., Tintorelli, R., Correa, J., Budriesi, P., & Viola, H. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15249 · Cited by 10
Non-Hebbian plasticity transforms transient experiences into lasting memories
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Intra‐amygdala metaplasticity modulation of fear extinction learning
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Behavioral and Cellular Tagging in Young and in Early Cognitive Aging
Gros, A., Lim, A. W. H., Hohendorf, V., White, N. C., Eckert, M. J., McHugh, T. J., & Wang, S. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.809879 · Cited by 11
“Familiar environment is shown to not improve memory retention (Ballarini et al., 2009; Wang et al., 2010).”
BackgroundAmnesia of inhibitory avoidance by scopolamine is overcome by previous open-field exposurePreprint
Colettis, N. C., Snitcofsky, M., Kornisiuk, E. E., Gonzalez, E. N., Quillfeldt, J. A., & Jerusalinsky, D. A. (2014) · Learning & Memory · doi:10.1101/lm.036210.114 · Cited by 11
“tion (Ballarini et al. 2009), while extinction of CFC was also promoted by exposure to a novel OF (de Carvalho Myskiw et al.”
BackgroundResultBehavioral tagging in infant ratsPreprint
Bae, S. E., & Richardson, R. (2018) · Learning & Memory · doi:10.1101/lm.047605.118 · Cited by 10
“iarization of the open field abolished the behavioral tagging effect (Ballarini et al. 2009; Moncada et al. 2011).”
BackgroundMethodResultInfluentialDefinition and exploitation of trends of evolution about interaction
Filippi, S., & Barattin, D. (2013) · Technological Forecasting and Social Change · doi:10.1016/j.techfore.2013.08.042 · Cited by 9
Psychosocial Modulators of Motor Learning in Parkinson’s Disease
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“…evidence for a neurobiological model called ‘‘tag-and-capture’’, which postulates that initially weak memories are strengthened through subsequent activation that engages common neural pathways minutes to hours later, through a synaptic mechanism (Frey and Morris, 1997; Ballarini et al., 2009).”
BackgroundPotent attenuation of context fear by extinction training contiguous with acquisitionPreprint
Bernier, B. E., Lacagnina, A. F., & Drew, M. R. (2014) · Learning & Memory · doi:10.1101/lm.036673.114 · Cited by 9
“…or impair long-term potentiation in the hippocampus (Xu et al. 1998; Abraham et al. 2002; Li et al. 2003; Straube et al. 2003; Davis et al. 2004) and can strengthen learning in a variety of hippocampus-dependent tasks (Moncada and Viola 2007; Ballarini et al. 2009; Almaguer-Melian et al. 2012).”
BackgroundRiboldi, J. G., Correa, J., Renfijes, M. M., Tintorelli, R., & Viola, H. (2024) · Communications Biology · doi:10.1038/s42003-024-06586-8 · Cited by 10
“Interestingly, here we observed that the promoting effect of the DHK infusion on the formationofSOR-LTMinducedbyawSORwassimilartothatdescribedfor thepromotingeffectinducedbyOF,occurringat − 2and + 2 hofthewSOR, but being ineffective at more distant times (Ballarini et al. 41 and Fig.”
Khan, R., Kulasiri, D., & Samarasinghe, S. (2022) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2022.111326 · Cited by 8
Behavioral tagging: Plausible involvement of PKMζ, Arc and role of neurotransmitter receptor systems
Vishnoi, S., Naseem, M., Raisuddin, S., & Parvez, S. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.009 · Cited by 8
“In the process of behavioral tagging, two separate events converge at a common population of neurons but of different nearby synapses of the same neuron in a critical time window (Ballarini et al., 2009).”
BackgroundSex and the facilitation of cued fear by prior contextual fear conditioning in ratsPreprint
Vazquez, K., Cole, K. E., & Parsons, R. G. (2024) · Learning & Memory · doi:10.1101/lm.054010.124 · Cited by 8
“…includes studies of “ behavioral tagging, ” where it has been shown that exploration of an open fi eld can facilitate learning of inhibitory avoidance when the two experiences are presented within a certain interval of each other (Moncada and Viola 2007; Moncada et al. 2011; Ballarini et al. 2009).”
Beyond boundaries: extended temporal flexibility in synaptic tagging and capture
Chong, Y. S., Ang, S. R., & Sajikumar, S. (2025) · Communications Biology · doi:10.1038/s42003-025-07998-w · Cited by 9
Van der Waals Epitaxy of CsPbI3/MoS2 Heterojunction Phototransistors for Neuromorphic Computing
Lu, R., Lu, C., Li, Y., Song, H., Gou, K., Yuan, X., & Jiang, J. (2025) · The Journal of Physical Chemistry Letters · doi:10.1021/acs.jpclett.5c02548 · Cited by 7
Modulation of memory reconsolidation by adjacent novel tasks: timing defines the nature of change
Schroeder, M. N., Fullio, C. L., Ballarini, F., & Moncada, D. (2023) · Communications Biology · doi:10.1038/s42003-023-05666-5 · Cited by 9
“This overlapping was higher than the one observed when the animals explored a familiar environment, which did not promote OR-memory consolidation through behavioral tagging 38 ; a lack of effect also shown in different learning tasks 11,18 .”
InfluentialOpen field exposure facilitates the expression of a spatial, recognition memory
Justel, N. R., Salguero, A., Marengo, L. G., Psyrdellis, M., & Pautassi, R. M. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.135997 · Cited by 7
Behavioural tagging: Effect of novelty exploration on plasticity related molecular signatures
Naseem, M., Vishnoi, S., Kaushik, M., & Parvez, S. (2021) · Experimental Brain Research · doi:10.1007/s00221-021-06099-4 · Cited by 7
Steiger, T. K., Sobczak, A., Reineke, R., & Bunzeck, N. (2022) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14750 · Cited by 6
Persistence of Spatial Memory Induced by Spaced Training Involves a Behavioral-Tagging Process
Correa, J., Tintorelli, R., Budriesi, P., & Viola, H. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.02.032 · Cited by 8
Neurocomunicación en videojuegos: llegando a un público sobreestimulado
Barrientos–Báez, A., & Domínguez, D. C. (2023) · TECHNO REVIEW International Technology Science and Society Review /Revista Internacional de Tecnología Ciencia y Sociedad · doi:10.37467/revtechno.v13.4809 · Cited by 7
“…hipótesis que luego puedan someterse a la lógica simulada del luego activa el proceso de etiquetado conceptual: un mecanismo neuronal que, al generarse una mayor actividad de síntesis proteica disparada por la experimentación de una vivencia novedosa, consolida la memoria (Ballarini et al ., 2009).”
States of epistemic curiosity interfere with memory for incidental scholastic facts
Keller, N. E., Salvi, C., Leiker, E., Gruber, M. J., & Dunsmoor, J. E. (2024) · npj Science of Learning · doi:10.1038/s41539-024-00234-w · Cited by 8
The future can shape memory for the present
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Wagner, I. C., van Buuren, M., Bovy, L., Morris, R., & Fernández, G. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4502-8 · Cited by 7
“The memory trace, however, is only stabilized and stored in long-term memory if these cellular events are accompanied by the synthesis of plasticity-related proteins (PRPs; Moncada and Viola 2007; Bekinschtein et al. 2008; Ballarini et al. 2009; Moncada et al. 2011).”
BackgroundFacilitation of fear learning by prior and subsequent fear conditioning
Lee, J., Russo, A. S., & Parsons, R. G. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.03.008 · Cited by 7
“that subsequent experience can enhance learning that has already occurred [13,14], and the time course of these enhancement effects have been shown to be restricted to a few hours, which our observation is”
Hypothesized Mechanisms of Cognitive Impairment During High-Intensity Acute Exercise
Jung, M., Kang, M., & Loprinzi, P. D. (2023) · Integrated science · doi:10.1007/978-3-031-15959-6_14 · Cited by 6
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“These processes ultimately initiate transcription, promoting the synthesis of essential proteins for the transformation of short-term memory into long-term memory in the behavioural tagging process [7, 8, 14, 76].”
BackgroundInfluentialActivity-Dependent Protein Transport as a Synaptic Tag
Okada, D., & Inokuchi, K. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1761-7_6 · Cited by 6
Memory Impairment after Drug-Facilitated Crimes
Saussereau, É., Guerbet, M., Anger, J.-P., & Goullé, J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-416748-3.00005-0 · Cited by 6
Novelty during a late postacquisition time window attenuates the persistence of fear memory
Katche, C., Tomaiuolo, M., Dorman, G. S., Medina, J. H., & Viola, H. (2016) · Scientific Reports · doi:10.1038/srep35220 · Cited by 6
Neuropsin‐dependent and ‐independent behavioral tagging
Suzuki, Y., Yoda, Y., & Ishikawa, Y. (2021) · Neuropsychopharmacology Reports · doi:10.1002/npr2.12177 · Cited by 5
Spatial memory and hippocampal enhancement
Peters, M., Muñoz, M., & Morris, R. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.03.005 · Cited by 6
de Andrade, C. V., Soliani, A. G., & Cerutti, S. M. (2023) · Learning & Memory · doi:10.1101/lm.053755.123 · Cited by 6
“Overlap in the population of neurons activated by conditioned and unconditioned stimuli was observed in Pavlovian conditioning and conditioned taste aversion (Ballarini et al. 2009; Moncada et al. 2015; Nomoto et al. 2016).”
BackgroundMethodInfluentialLima, K. R., Alves, N., Lopes, L. F., Picua, S. S., de Vargas, L. D. S., Daré, L. R., Ramborger, B. P., Roehrs, R., de Gomes, M. G., & Mello‐Carpes, P. B. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110832 · Cited by 5
Leite, A. K. O., Farias, C. P., Schmidt, B. E., Teixeira, L., Rieder, A. S., Furini, C. R. G., & Wyse, Â. T. D. S. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.10.016 · Cited by 6
The penumbra of learning: A statistical theory of synaptic tagging and capture
Gershman, S. J. (2014) · Network Computation in Neural Systems · doi:10.3109/0954898x.2013.862749 · Cited by 5
“For example, learning in a variety of tasks (spatial object recognition, contextual fear conditioning, conditioned taste aversion) can be enhanced by allowing animals to explore a novel spatial environment before or after training (Ballarini et al., 2009).”
BackgroundEl poder educativo de lo inesperado. Estudio de experiencias innovadoras en la universidad
Melgar, M. F., Elisondo, R. C., Donolo, D., & Stoll, R. G. (2016) · Cuadernos de Investigación Educativa · doi:10.18861/cied.2016.7.2.2609 · Cited by 5
High-Throughput Task to Study Memory Recall During Spatial Navigation in Rodents
Morales, L., Tomàs, D. P., Dalmau, J. O., de la Rocha, J., & Jercog, P. E. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00064 · Cited by 7
“Another widely used task to test spatial memory is the spatial object recognition (SOR) task (Ballarini et al., 2009).”
BackgroundA meta-analysis of the effect of protein synthesis inhibitors on rodent fear conditioning
Carneiro, C. F. D., Amorim, F. E., & Amaral, O. B. (2023) · Peer Community Journal · doi:10.24072/pcjournal.339 · Cited by 7
Reward anticipation modulates the effect of stress-related increases in cortisol on episodic memory
Quent, J. A., McCullough, A. M., Sazma, M. A., Wolf, O. T., & Yonelinas, A. P. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.11.007 · Cited by 5
“Based on tag-and-capture models (Ballarini et al., 2009; Frey & Morris, 1997; Moncada & Viola, 2007; Redondo & Morris, 2011; Viola et al., 2014; Wang et al., 2010), we predicted that stress would benefit memory for the non-reward items, but would have less of a beneficial effect for reward items.”
MethodReward-enhanced encoding improves relearning of forgotten associations
Lombard, E., Ciucci, S., Cannistraci, C. V., Bavelier, D., & Schwartz, S. (2018) · Scientific Reports · doi:10.1038/s41598-018-26929-w · Cited by 4
Hippocampal Arc Induces Decay of Object Recognition Memory in Male Mice
Shandilya, M., & Gautam, A. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.02.012 · Cited by 5
Emotion–Cognition Interactions in Memory and Decision Making
Speer, M. E., & Delgado, M. R. (2018) · Wiley eBooks · doi:10.1002/9781119170174.epcn418 · Cited by 5
Clewett, D., Dunsmoor, J. E., Bachman, S. L., Phelps, E. A., & Davachi, L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.07.192252 · Cited by 5
“Building on a series of experiments in rodents, the behavioral tagging model posits that a weak memory trace can be strengthened by a stronger, arousing event that engages the same neural pathways (Ballarini et al., 2009; Moncada & Viola, 2007).”
BackgroundInfluentialLiu, Q., Wang, H., Lin, J.-T., Jiao, X., Liu, Y., Li, T., Xie, Z., Zhou, C., Wu, Y.-Q., & Miao, H. (2025) · British Journal of Anaesthesia · doi:10.1016/j.bja.2024.11.045 · Cited by 4
The Molecular Substrates of Second-Order Conditioned Fear in the Basolateral Amygdala Complex
Leake, J., Shvetcov, A., Clemens, K. J., Kershaw, K. A., Westbrook, R. F., & Holmes, N. M. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1087-24.2025 · Cited by 4
Experience‐driven competition in neural reorganization after stroke
Jones, T. A., Nemchek, V., & Fracassi, M. (2024) · The Journal of Physiology · doi:10.1113/jp285565 · Cited by 4
“A proximal experience (a novel taste) that promoted PRP synthesis in insular cortex increased the long-term expression of a weakly learned version of conditioned taste aversion (Ballarini et al., 2009).”
A Mechanism of Synaptic Clock Underlying Subjective Time Perception
Jura, B. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00716 · Cited by 4
“It has been proposed to underlie a short-lasting memory of behavioral events (Ballarini et al., 2009; Wang et al., 2010).”
BackgroundIs there selective retroactive memory enhancement in humans?: a meta-analysis
Koevoet, D., & Postma, A. (2023) · Psychonomic Bulletin & Review · doi:10.3758/s13423-023-02372-5 · Cited by 7
“The behavioral tagging hypothesis has extended the cellular principles from the synaptic tag-and-capture hypothesis to learning and memory (Ballarini et al., 2009; Moncada et al., 2015).”
InfluentialNovelty exposure hinders aversive memory generalization and depends on hippocampal protein synthesis
de Vargas, L. D. S., Sevenster, D., Lima, K. R., Izquierdo, I., D’Hooge, R., & Mello‐Carpes, P. B. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.10.034 · Cited by 4
Cole, K. E., Lee, J., Davis, M., & Parsons, R. G. (2019) · eNeuro · doi:10.1523/eneuro.0113-19.2019 · Cited by 4
“For example, motivated by in vitro studies of synaptic tagging and capture, several studies have reported that relatively innocuous experiences that normally produce only transient memories can be transformed into robust long-term memory (LTM) if another experience had occurred near in time (Moncada and Viola, 2007; B…”
BackgroundThe Role of Synaptic Tagging and Capture for Memory Dynamics in Spiking Neural Networks
Luboeinski, J. (2021) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-463 · Cited by 4
Lima, K. R., das Neves, B.-H. S., Sigaran, G. J., da Rosa, A. C. D. S., Gomes, G. C. M., de Gomes, M. G., & Mello‐Carpes, P. B. (2024) · Neurochemistry International · doi:10.1016/j.neuint.2024.105740 · Cited by 4
Linking new information to a short-lasting memory trace induces consolidation in the hippocampus
Soliani, A. G., Baptista, J. S., Muratori, B. G., Armelin‐Correa, L., & Cerutti, S. M. (2024) · iScience · doi:10.1016/j.isci.2024.111320 · Cited by 3
“These findings confirm the existence of a critical temporal window for novelty-induced memory enhancements, as previously reported 5,6 .”
InfluentialTezanos, P., & Trejo, J. L. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106145 · Cited by 3
“…2022), which seeks to explain how pre-training exposure to neutral novelty or a stressor facilitates memory formation across various forms of learning (Ballarini et al., 2009; Lopes da Cunha et al., 2022; Budriesi et al., 2023), including naturalistic human behavior (Ramirez Butavand et al., 2020).”
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
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