Behavioral tagging is a general mechanism of long-term memory formation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 34, 2009, Pages 14599-14604

  Ballarini, Fabricio ^a   Moncada, Diego ^a   Martinez, Maria Cecilia ^a   Alen, Nadia ^a   Viola, Haydée ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Hippocampus; Insular cortex; Memory consolidation; Novelty; Protein synthesis

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONDITIONED REFLEX; CONDITIONING; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MALE; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; RECOGNITION; SHORT TERM MEMORY; TASK PERFORMANCE; TASTE AVERSION; TRAINING;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); DISCRIMINATION LEARNING; FEAR; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MALE; MEMORY; MEMORY, SHORT-TERM; NEOCORTEX; NEURONAL PLASTICITY; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR; SACCHARIN; SODIUM CHLORIDE; SPATIAL BEHAVIOR; TASTE; TIME FACTORS;

RATTUS;

EID: 70149090622     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0907078106     Document Type: Article

References (37)

1. Costa-Mattioli M, Sonenberg N (2008) Translational control of gene expression: A molecular switch for memory storage. Prog Brain Res 169:81-95.
2. Moncada D, Viola H (2007) Induction of long-term memory by exposure to novelty requires protein synthesis: Evidence for a behavioral tagging. J Neurosci 27:7476-7481. (Pubitemid 47066574)
3. Hebb D, ed (1949) The Organization of Behavior: A Neuropsychological Theory (Wiley, New York).
4. Konorski J, ed (1948) Conditioned Reflexes and Neuron Organization (Cambridge Univ Press, Cambridge, UK).
5. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23:649-711. (Pubitemid 30350057)
6. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
7. Barco A, Lopez de Armentia M, Alarcon JM (2008) Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited 10 years later. Neurosci Biobehav Rev 32:831-851.
8. Frey S, Frey JU (2008) "Synaptic tagging" and "cross-tagging" and related associative reinforcement processes of functional plasticity as the cellular basis for memory formation. Prog Brain Res 169:117-143.
9. Govindarajan A, Kelleher RJ, Tonegawa S (2006) A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci 7:575-583. (Pubitemid 43989775)
10. Straube T, Korz V, Balschun D, Frey JU (2003) Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J Physiol 552(Pt 3):953-960. (Pubitemid 37428433)
11. Uzakov S, Frey JU, Korz V (2005) Reinforcement of rat hippocampal LTP by holeboard training. Learn Mem 12:165-171. (Pubitemid 40517084)
12. Izquierdo I, et al. (2006) Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci 29:496-505. (Pubitemid 44291818)
13. Berman DE, Dudai Y (2001) Memory extinction, learning anew, and learning the new: Dissociations in the molecular machinery of learning in cortex. Science 291:2417-2419.
14. Bermudez-Rattoni F (2004) Molecular mechanisms of taste-recognition memory. Nat Rev Neurosci 5:209-217.
15. ReymannKG,FreyJU(2007)ThelatemaintenanceofhippocampalLTP:Requirements, phases, 'synaptic tagging', 'late-associativity' and implications. Neuropharmacology 52:24-40.
16. Frey U, Morris RG (1998) Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21:181-188. (Pubitemid 28191809)
17. Frey U, Morris RG (1998) Weak before strong: Dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545-552. (Pubitemid 28306943)
18. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677.
19. Mumby DG, Gaskin S, Glenn MJ, Schramek TE, Lehmann H (2002) Hippocampal damage and exploratorypreferencesin rats:Memoryfor objects, places,andcontexts. LearnMem9:49-57. (Pubitemid 34507491)
20. Bermudez-Rattoni F, McGaugh JL (1991) Insular cortex and amygdala lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion. Brain Res 549:165-170.
21. Sajikumar S, Frey JU (2004) Resetting of "synaptic tags" is time- and activity-dependent in rat hippocampal CA1 in vitro. Neuroscience 129:503-507. (Pubitemid 39388869)
22. Young JZ, Isiegas C, Abel T, Nguyen PV (2006) Metaplasticity of the late-phase of long-term potentiation: A critical role for protein kinase A in synaptic tagging. Eur J Neurosci 23:1784-1794.
23. Young JZ, Nguyen PV (2005) Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity. J Neurosci 25:7221-7231.
24. Chrivia JC, et al. (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855-859. (Pubitemid 23341031)
25. Matsuo N, Reijmers L, Mayford M (2008) Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 319:1104-1107. (Pubitemid 351300794)
26. Sajikumar S, Navakkode S, Sacktor TC, Frey JU (2005) Synaptic tagging and crosstagging: The role of protein kinase Mzeta in maintaining long-term potentiation but not long-term depression. J Neurosci 25:5750-5756. (Pubitemid 40847887)
27. Alonso M, Medina JH, Pozzo-Miller L (2004) ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn Mem 11:172-178. (Pubitemid 38456599)
28. Alonso M, et al. (2002) BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12:551-560. (Pubitemid 34906483)
29. Tanaka J, et al. (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319:1683-1687.
30. Lu Y, Christian K, Lu B (2008) BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89:312-323. (Pubitemid 351318269)
31. Bekinschtein P, et al. (2007) Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 53:261-277. (Pubitemid 46074403)
32. Bekinschtein P, et al. (2008) BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci USA 105:2711-2716.
33. Moguel-Gonzalez M, Gomez-Palacio-Schjetnan A, Escobar ML (2008) BDNF reverses the CTA memory deficits produced by inhibition of protein synthesis. Neurobiol Learn Mem 90:584-587.
34. Moncada D, Viola H (2006) Phosphorylation state of CREB in the rat hippocampus: A molecular switch between spatial novelty and spatial familiarity? Neurobiol Learn Mem 86:9-18. (Pubitemid 43776634)
35. Moncada D, Viola H (2008) PKMzeta inactivation induces spatial familiarity. Learn Mem 15:810-814.
36. Sweatt JD (1999) Toward a molecular explanation for long-term potentiation. Learn Mem 6:399-416.
37. Miranda MI, Ferreira G, Ramirez-Lugo L, Bermudez-Rattoni F (2002) Glutamatergic activity in the amygdala signals visceral input during taste memory formation. Proc Natl Acad Sci USA 99:11417-11422. (Pubitemid 34920940)