Artículo

Viola, H.; Ballarini, F.; Martínez, M.C.; Moncada, D. "The tagging and capture hypothesis from synapse to memory" (2014) Progress in Molecular Biology and Translational Science. 122:391-423
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The synaptic tagging and capture theory (STC) was postulated by Frey and Morris in 1997 and provided a strong framework to explain how to achieve synaptic specificity and persistence of electrophysiological-induced plasticity changes. Ten years later, the same argument was applied on learning and memory models to explain the formation of long-term memories, resulting in the behavioral tagging hypothesis (BT). These hypotheses are able to explain how a weak event that induces transient changes in the brain can establish long-lasting phenomena through a tagging and capture process. In this framework, it was postulated that the weak event sets a tag that captures plasticity-related proteins/products (PRPs) synthesized by an independent strong event. The tagging and capture processes exhibit symmetry, and therefore, PRPs can be captured if they are synthesized either before or after the setting of the tag. In summary, the hypothesis provides a wide framework that gives a solid explanation of how lasting changes occur and how the interaction between different events leads to promotion, reinforcement, or impairment of such changes. In this chapter, we will summarize the postulates of STC hypothesis, the common features between synaptic plasticity and memory, as well as a detailed compilation of the findings supporting the existence of BT process. At the end, we pose some questions related to BT mechanism and LTM formation, which probably will be answered in the near future. © 2014 Elsevier Inc.

Registro:

Documento: Artículo
Título:The tagging and capture hypothesis from synapse to memory
Autor:Viola, H.; Ballarini, F.; Martínez, M.C.; Moncada, D.
Filiación:Instituto de Biología Celular y Neurociencias Prof. E. de Robertis, Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Fisiología, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Neurophysiology of Learning and Memory Research Group, Leibniz-Institut für Neurobiologie, Magdeburg, Germany
Palabras clave:Behavioral tagging hypothesis; Long-term memory formation; Rodents and human beings; Synaptic and capture hypothesis; Synaptic plasticity and memory; article; behavior; behavioral tagging; brain; fear; human; hypothesis; learning; long term memory; nerve cell plasticity; nonhuman; protein synthesis; reinforcement; spatial memory; synapse; tagging and capture theory; task performance; Behavioral tagging hypothesis; Long-term memory formation; Rodents and human beings; Synaptic and capture hypothesis; Synaptic plasticity and memory; Animals; Brain; Gene Expression Regulation; Humans; Memory; Neuronal Plasticity; Synapses
Año:2014
Volumen:122
Página de inicio:391
Página de fin:423
DOI: http://dx.doi.org/10.1016/B978-0-12-420170-5.00013-1
Título revista:Progress in Molecular Biology and Translational Science
Título revista abreviado:Prog. Mol. Biol. Transl. Sci.
ISSN:18771173
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_18771173_v122_n_p391_Viola

Referencias:

  • Frey, U., Morris, R.G., Synaptic tagging and long-term potentiation (1997) Nature, 385, pp. 533-536
  • Moncada, D., Viola, H., Induction of long-term memory by exposure to novelty requires protein synthesis: Evidence for a behavioral tagging (2007) J Neurosci, 27, pp. 7476-7481
  • Martin, K.C., Kosik, K.S., Synaptic tagging - Who's it? (2002) Nat Rev Neurosci, 3, pp. 813-820
  • Kelleher, R.J., Govindarajan, A., Tonegawa, S., Translational regulatory mechanisms in persistent forms of synaptic plasticity (2004) Neuron, 44 (1), pp. 59-73
  • Lu, Y., Christian, K., Lu, B., BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory? (2008) Neurobiol Learn Mem, 89 (3), pp. 312-323
  • Lu, Y., Ji, Y., Ganesan, S., TrkB as a potential synaptic and behavioral tag (2011) J Neurosci, 31, pp. 11762-11771
  • Moncada, D., Ballarini, F., Martinez, M.C., Frey, J.U., Viola, H., Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation (2011) Proc Natl Acad Sci USA, 108, pp. 12931-12936
  • De Carvalho Myskiw, J., Benetti, F., Izquierdo, I., Behavioral tagging of extinction learning (2013) Proc Natl Acad Sci USA, 110 (3), pp. 1071-1076
  • Frey, S., Frey, J.U., "synaptic tagging" and "cross-tagging" and related associative reinforcement process of functional plasticity as the celular basis of memory formation (2008) Prog Brain Res, 169, pp. 117-143
  • Ramachandran, B., Frey, J.U., Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro (2009) J Neurosci, 29 (39), pp. 12167-12173
  • Redondo, R.L., Morris, R.G.M., Making memories last: The synaptic tagging and capture hypothesis (2011) Nat Rev Neurosci, 12, pp. 17-30
  • Sajikumar, S., Navakkode, S., Frey, J.U., Identification of compartment- and process-specific molecules required for "synaptic tagging" during long-term potentiation and long-term depression in hippocampal CA1 (2007) J Neurosci, 27 (19), pp. 5068-5080
  • Redondo, R.L., Okuno, H., Spooner, P.A., Frenguelli, B.G., Bito, H., Morris, R.G., Synaptic tagging and capture: Differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation (2010) J Neurosci, 30 (14), pp. 4981-4989
  • Martin, S.J., Morris RG new life in an old idea: The synaptic plasticity and memory hypothesis revisited (2002) Hippocampus, 12 (5), pp. 609-636
  • Martin, S.J., Grimwood, P.D., Morris, R.G., Synaptic plasticity and memory: An evaluation of the hypothesis (2000) Annu Rev Neurosci, 23, pp. 649-711
  • Whitlock, J.R., Heynen, A.J., Shuler, M.G., Bear, M.F., Learning induces long-term potentiation in the hippocampus (2006) Science, 313, pp. 1093-1097
  • Gruart, A., Muñoz, M.D., Delgado-García, J.M., Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice (2006) J Neurosci, 26 (4), pp. 1077-1087
  • Green, E.J., Greenough, W.T., Altered synaptic transmission in dentate gyrus of rats reared in complex environments: Evidence from hippocampal slices maintained in vitro (1986) J Neurophysiol, 55 (4), pp. 739-750
  • Rioult-Pedotti, M.S., Friedman, D., Hess, G., Donoghue, J.P., Strengthening of horizontal cortical connections following skill learning (1998) Nat Neurosci, 1 (3), pp. 230-234
  • Saar, D., Grossman, Y., Barkai, E., Reduced synaptic facilitation between pyramidal neurons in the piriform cortex after odor learning (1999) J Neurosci, 19 (19), pp. 8616-8622
  • Clarke, J.R., Cammarota, M., Gruart, A., Izquierdo, I., Delgado-García, J.M., Plastic modifications induced by object recognition memory processing (2010) Proc Natl Acad Sci USA, 107 (6), pp. 2652-2657
  • Goh, J.J., Manahan-Vaughan, D., Spatial object recognition enables endogenous LTD that curtails LTP in the mouse hippocampus (2013) Cereb Cortex, 23 (5), pp. 1118-1125. , 10.1093/cercor/bhs089
  • Griffiths, S., Scott, H., Glover, C., Expression of long-term depression underlies visual recognition memory (2008) Neuron, 58 (2), pp. 186-194
  • Seoane, A., Massey, P.V., Keen, H., Bashir, Z.I., Brown, M.W., L-type voltage-dependent calcium channel antagonists impair perirhinal long-term recognition memory and plasticity processes (2009) J Neurosci, 29 (30), pp. 9534-9544
  • Ge, Y., Dong, Z., Bagot, R.C., Hippocampal long-term depression is required for the consolidation of spatial memory (2010) Proc Natl Acad Sci USA, 107, pp. 16697-16702
  • Dong, Z., Gong, B., Li, H., Mechanisms of hippocampal long-term depression are required for memory enhancement by novelty exploration (2012) J Neurosci, 32 (35), pp. 11980-11990
  • Frey, U., Morris, R.G., Weak before strong: Dissociating synaptic tagging and plasticity-factor accounts of late-LTP (1998) Neuropharmacology, 37 (45), pp. 545-552
  • Young, J.Z., Nguyen, P.V., Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity (2005) J Neurosci, 25 (31), pp. 7221-7231
  • Sajikumar, S., Frey, J.U., Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD (2004) Neurobiol Learn Mem, 82 (1), pp. 12-25
  • Sajikumar, S., Navakkode, S., Sacktor, T.C., Frey, J.U., Synaptic tagging and cross-tagging: The role of protein kinase Mzeta in maintaining long-term potentiation but not long-term depression (2005) J Neurosci, 25 (24), pp. 5750-5756
  • Kauderer, B.S., Kandel, E.R., Capture of a protein synthesis-dependent component of long-term depression (2000) Proc Natl Acad Sci USA, 97 (24), pp. 13342-13347
  • Govindarajan, A., Kelleher, R.J., Tonegawa, S., A clustered plasticity model of long-term memory engrams (2006) Nat Rev Neurosci, 7 (7), pp. 575-583
  • Sajikumar, S., Korte, M., Metaplasticity governs compartmentalization of synaptic tagging and capture through brain-derived neurotrophic factor (BDNF) and protein kinase Mzeta (PKMzeta) (2011) Proc Natl Acad Sci USA, 108 (6), pp. 2551-2556
  • Frey, U., Morris, R.G., Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation (1998) Trends Neurosci, 21, pp. 181-188
  • Shires, K.L., Da Silva, B.M., Hawthorne, J.P., Morris, R.G., Martin, S.J., Synaptic tagging and capture in the living rat (2012) Nat Commun, 3, p. 1246
  • Frey, S., Bergado-Rosado, J., Seidenbecher, T., Pape, H.C., Frey, J.U., Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: Heterosynaptic induction mechanisms of late-LTP (2001) J Neurosci, 21, pp. 3697-3703
  • Straube, T., Frey, J.U., Involvement of beta-adrenergic receptors in protein synthesis-dependent late long-term potentiation (LTP) in the dentate gyrus of freely moving rats: The critical role of the LTP induction strength (2003) Neuroscience, 119 (2), pp. 473-479
  • Bergado, J.A., Frey, S., López, J., Almaguer-Melian, W., Frey, J.U., Cholinergic afferents to the locus coeruleus and noradrenergic afferents to the medial septum mediate LTP-reinforcement in the dentate gyrus by stimulation of the amygdala (2007) Neurobiol Learn Mem, 88 (3), pp. 331-341
  • Bergado, J.A., Scherf, T., Almaguer-Melian, W., Frey, S., López, J., Frey, J.U., Stimulation of the nucleus raphe medialis modifies basal synaptic transmission at the dentate gyrus, but not long-term potentiation or its reinforcement by stimulation of the basolateral amygdala (2009) Neurosci Lett, 464 (3), pp. 179-183
  • Almaguer-Melian, W., Bergado, J.A., Martínez-Martí, L., Duany-Machado, C., Frey, J.U., Basolateral amygdala stimulation does not recruit LTP at depotentiated synapses (2012) Physiol Behav, 101 (4), pp. 549-553
  • Reymann, K.G., Frey, J.U., The late maintenance of hippocampal LTP: Requirements, phases, 'synaptic tagging', 'late-associativity' and implications (2007) Neuropharmacology, 52 (1), pp. 24-40
  • Li, S., Cullen, W.K., Anwyl, R., Rowan, M.J., Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty (2003) Nat Neurosci, 6 (5), pp. 526-531
  • Davis, C.D., Jones, F.L., Derrick, B.E., Novel environments enhance the induction and maintenance of long-term potentiation in the dentate gyrus (2004) J Neurosci, 24 (29), pp. 6497-6506
  • Straube, T., Korz, V., Balschun, D., Frey, J.U., Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus (2003) J Physiol, 552, pp. 953-960
  • Corrêa, S.A., Hunter, C.J., Palygin, O., MSK1 regulates homeostatic and experience-dependent synaptic plasticity (2012) J Neurosci, 32 (38), pp. 13039-13051
  • Seidenbecher, T., Balschun, D., Reymann, K.G., Drinking after water deprivation prolongs "unsaturated" LTP in the dentate gyrus of rats (1995) Physiol Behav, 57 (5), pp. 1001-1004
  • Seidenbecher, T., Reymann, K.G., Balschun, D., A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli (1997) Proc Natl Acad Sci USA, 94 (4), pp. 1494-1499
  • Bergado, J.A., Almaguer-Melian, W., Kostenko, S., Frey, S., Frey, J.U., Behavioral reinforcement of long-term potentiation in rat dentate gyrus in vivo is protein synthesis-dependent (2003) Neurosci Lett, 351 (1), pp. 56-58
  • Uzakov, S., Frey, J.U., Korz, V., Reinforcement of rat hippocampal LTP by holeboard training (2005) Learn Mem, 12 (2), pp. 165-171
  • Korz, V., Frey, J.U., Emotional and cognitive reinforcement of rat hippocampal long-term potentiation by different learning paradigms (2004) Neuron Glia Biol, 1 (3), pp. 253-261
  • Moncada, D., Frey, J., The effects of LTP induction on hippocampus-dependent memories: Synaptic and behavioral tagging (2011) Society for Neuroscience Meeting November 2011, San Diego, USA
  • Viola, H., Furman, M., Izquierdo, L., Phosphorylated cAMP response element-binding protein as a molecular marker of memory processing in rat hippocampus: Effect of novelty (2000) J Neurosci, 20, p. 112
  • Winograd, M., Viola, H., Detection of novelty, but not memory of spatial habituation, is associated with an increase in phosphorylated cAMP response element-binding protein levels in the hippocampus (2004) Hippocampus, 14, pp. 117-123
  • Moncada, D., Viola, H., Phosphorylation state of CREB in the rat hippocampus: A molecular switch between spatial novelty and spatial familiarity? (2006) Neurobiol Learn Mem, 86, pp. 9-18
  • Straube, T., Korz, V., Frey, J., Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus (2003) Neurosci Lett, 344, pp. 5-8
  • Izquierdo, I., Bevilaqua, L., Rossato, J., Bonini, J., Medina, J., Cammarota, M., Different molecular cascades in different sites of the brain control memory consolidation (2006) Trends Neurosci, 29, pp. 496-505
  • Ballarini, F., Moncada, D., Martinez, M.C., Alen, N., Viola, H., Behavioral tagging is a general mechanism of long-term memory formation (2009) Proc Natl Acad Sci USA, 106 (34), pp. 14599-14604
  • Kessels, R., Jaap Kappelle, L., De Haan, E.H., Postma, A., Lateralization of spatial-memory processes: Evidence on spatial span, maze learning, and memory for object locations (2000) Neuropsychologia, 40, pp. 1465-1473
  • Squire, L., Memory and hippocampus: A synthesis from findings with rats, monkeys, and humans (1992) Psychol Rev, 99, pp. 195-231
  • O'Keefe, J., Nadel, L., (1978) The Hippocampus As A Cognitive Map, , Oxford University Press London
  • Dix, S.F., Aggleton, J.P., Extending the spontaneous preference test of recognition: Evidence of object-location and object-context recognition (1999) Behav Brain Res, 99 (2), pp. 191-200
  • Mumby, D.G., Gaskin, S., Glenn, M.J., Schramek, T.E., Lehmann, H., Hippocampal damage and exploratory preferences in rats: Memory for objects, places, and contexts (2002) Learn Mem, 9 (2), pp. 49-57
  • Wang, S.H., Redondo, R.L., Morris, R.G.M., Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory (2010) Proc Natl Acad Sci USA, 107, pp. 19537-19542
  • Almaguer-Melian, W., Bergado-Rosado, J., Pavón-Fuentes, N., Alberti-Amador, E., Mercerón-Martínez, D., Frey, U., Novelty exposure overcomes foot shock-induced spatial-memory impairment by processes of synaptic-tagging in rats (2012) Proc Natl Acad Sci USA, 109 (3), pp. 953-958
  • Aggleton, J.P., Brown, M.W., Episodic memory, amnesia, and the hippocampal-anterior thalamic axis (1999) Behav Brain Sci, 22 (3), pp. 425-444
  • Warburton, E.C., Brown, M.W., Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory (2010) Neuropsychologia, 48 (8), pp. 2262-2272
  • Berman, D.E., Dudai, Y., Memory extinction, learning anew, and learning the new: Dissociations in the molecular machinery of learning in cortex (2001) Science, 291, pp. 2417-2419
  • Merhav, M., Rosemblum, K., Facilitation of taste memory acquisition by experiencing previous novel taste is protein-synthesis dependent (2008) Learn Mem, 15 (7), pp. 501-507
  • Lisman, J.E., Grace, A.A., The hippocampal-VTA loop: Controlling the entry of information into long-term memory (2005) Neuron, 46 (5), pp. 703-713
  • Kitchigina, V., Vankov, A., Harley, C., Sara, S.J., Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus (1997) Eur J Neurosci, 9 (1), pp. 41-47
  • Sara, S.J., Vankov, A., Hervé, A., Locus coeruleus-evoked responses in behaving rats: A clue to the role of noradrenaline in memory (1994) Brain Res Bull, 35, pp. 457-465
  • Vankov, A., Hervé-Minvielle, A., Sara, S.J., Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat (1995) Eur J Neurosci, 7, pp. 1180-1187
  • Gao, C., Gill, M.B., Tronson, N.C., Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation (2010) Hippocampus, 20 (9), pp. 1072-1082
  • Cammarota, M., De Stein, M.L., Paratcha, G., Bevilaqua, L.R., Izquierdo, I., Medina, J.H., Rapid and transient learning-associated increase in NMDA NR1 subunit in the rat hippocampus (2000) Neurochem Res, 25 (5), pp. 567-572
  • Im, H.I., Nakajima, A., Gong, B., Post-training dephosphorylation of eEF-2 promotes protein synthesis for memory consolidation (2009) PLoS One, 4, p. 7424
  • McGaugh, J.L., Memory - A century of consolidation (2000) Science, 287 (5451), pp. 248-251
  • Moncada, D., Martinez, M.C., Ballarini, F., Alen, N., Viola, H., In the search for the behavioral tag (2008) Society for Neuroscience Meeting November 2008, Washington, USA
  • Pastalkova, E., Serrano, P., Pinkhasova, D., Wallace, E., Fenton, A.A., Sacktor, T.C., Storage of spatial information by the maintenance mechanism of LTP (2006) Science, 313, pp. 1141-1144
  • Volk, L.J., Bachman, J.L., Johnson, R., Yu, Y., Huganir, R.L., PKM-ζ is not required for hippocampal synaptic plasticity, learning and memory (2013) Nature, 493, pp. 420-423
  • Navakkode, S., Sajikumar, S., Frey, J.U., Mitogen-activated protein kinase-mediated reinforcement of hippocampal early long-term depression by the type IV-specific phosphodiesterase inhibitor rolipram and its effect on synaptic tagging (2005) J Neurosci, 25, pp. 10664-10670
  • Martinez, M.C., Alen, N., Ballarini, F., Moncada, D., Viola, H., Memory traces compete under regimes of limited Arc protein synthesis: Implications for memory interference (2012) Neurobiol Learn Mem, 98, pp. 165-173
  • Sajikumar, S., Frey, J.U., Resetting of 'synaptic tags' is time- and activity-dependent in rat hippocampal CA1 in vitro (2004) Neuroscience, 129, pp. 503-507
  • Fonseca, R., Nägerl, U.V., Morris, R.G.M., Bonhoeffer, T., Competing for memory: Hippocampal LTP under regimes of reduced protein synthesis (2004) Neuron, 44, pp. 1011-1020
  • Govindarajan, A., Israely, I., Huang, S.-Y., Tonegawa, S., The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP (2011) Neuron, 69, pp. 132-146
  • Won, J., Silva, A.J., Molecular and cellular mechanisms of memory allocation in neuronetworks (2008) Neurobiol Learn Mem, 89, pp. 285-292
  • Yasuda, M., Johnson-Venkatesh, E., Multiple forms of activity-dependent competition refine hippocampal circuits in vivo (2011) Neuron, 70, pp. 1128-1142
  • Garagnani, M., Wennekers, T., Pulvermüller, F., Recruitment and consolidation of cell assemblies for words by way of Hebbian learning and competition in a multi-layer neural network (2009) Cognit Comput, 1, pp. 160-176
  • Bramham, C.R., Local protein synthesis, actin dynamics, and LTP consolidation (2008) Curr Opin Neurobiol, 18, pp. 524-531
  • Tzingounis, A.V., Nicoll, R., Arc/Arg3.1: Linking gene expression to synaptic plasticity and memory (2006) Neuron, 52, pp. 403-407
  • Wibrand, K., Pai, B., Siripornmongcolchai, T., MicroRNA regulation of the synaptic plasticity-related gene Arc (2012) PLoS One, 7, p. 41688
  • Bramham, C.R., Alme, M.N., Bittins, M., The Arc of synaptic memory (2011) Exp Brain Res, 200, pp. 125-140
  • Okuno, H., Akashi, K., Ishii, Y., Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ (2012) Cell, 149, pp. 886-898
  • Barco, A., Lopez De Armentia, M., Alarcon, J.M., Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited 10 years later (2008) Neurosci Biobehav Rev, 32, pp. 831-851
  • Jost, A., Die Assoziationsfestigkeit in ihrer Abhängigkeit von der Verteilung der Wiederholungen [The strength of associations in their dependence on the distribution of repetitions] (1897) Z Psychol., 14, pp. 436-472
  • Müller, G.E., Pilzecker, A., Experimentelle Beiträge zur Lehre vom Gedächtniss (1900) Z. Psychol. Ergänzungsband, 1, pp. 1-300
  • Ribot, T., (1881) Les Maladies de la Memoire (Diseases of Memory), , Appleton-Century-Crofts New York
  • Skaggs, E.B., Further studies in retroactive inhibition (1925) Psychol Monogr, 161, pp. 1-60
  • Ballarini, F., Martínez, M.C., Díaz Perez, M., Moncada, D., Viola, H., Memory in elementary school children is improved by an unrelated novel experience (2013) PLoS One, 8 (6), p. 66875
  • Rey, A., (1959) Test de Copie et de Reproduction de Memoire de Figures Geometriques Complexes [A Test of Copy and Recall of A Complex Geometric Figure], , Editions du centre de Psycholegie Appliquee
  • Li, Q., Rothkegel, M., Cheng Xiao, Z., Abraham, W., Korte, M., Sajikumar, S., Making synapses strong: Metaplasticity prolongs associativity of long-term memory by switching synaptic tag mechanisms (2012) Cereb Cortex, , 10.1093/cercor/bhs315

Citas:

---------- APA ----------
Viola, H., Ballarini, F., Martínez, M.C. & Moncada, D. (2014) . The tagging and capture hypothesis from synapse to memory. Progress in Molecular Biology and Translational Science, 122, 391-423.
http://dx.doi.org/10.1016/B978-0-12-420170-5.00013-1
---------- CHICAGO ----------
Viola, H., Ballarini, F., Martínez, M.C., Moncada, D. "The tagging and capture hypothesis from synapse to memory" . Progress in Molecular Biology and Translational Science 122 (2014) : 391-423.
http://dx.doi.org/10.1016/B978-0-12-420170-5.00013-1
---------- MLA ----------
Viola, H., Ballarini, F., Martínez, M.C., Moncada, D. "The tagging and capture hypothesis from synapse to memory" . Progress in Molecular Biology and Translational Science, vol. 122, 2014, pp. 391-423.
http://dx.doi.org/10.1016/B978-0-12-420170-5.00013-1
---------- VANCOUVER ----------
Viola, H., Ballarini, F., Martínez, M.C., Moncada, D. The tagging and capture hypothesis from synapse to memory. Prog. Mol. Biol. Transl. Sci. 2014;122:391-423.
http://dx.doi.org/10.1016/B978-0-12-420170-5.00013-1