Hippocampal molecular mechanisms involved in the enhancement of fear extinction caused by exposure to novelty

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

Volumn 111, Issue 12, 2014, Pages 4572-4577

  De Carvalho Myskiw, Jociane ^a   Furini, Cristiane Regina Guerino ^a   Benetti, Fernando ^a   Izquierdo, Ivan ^a  

^a PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Fear conditioning; Hippocampus; Memory; Synaptic plasticity; Synaptic tagging and capture

Indexed keywords

2 AMINO 5 PHOSPHONO PENTANOIC ACID; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; LACTACYSTIN BETA LACTONE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NIFEDIPINE; PHOSPHONIC ACID DERIVATIVE; PROTEASOME; RAPAMYCIN; UNCLASSIFIED DRUG; VALERIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG INFUSION; ENVIRONMENTAL EXPOSURE; FEAR; HIPPOCAMPUS; INFUSION; MALE; MOLECULAR MECHANICS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT;

FEAR CONDITIONING; HIPPOCAMPUS; MEMORY; SYNAPTIC PLASTICITY; SYNAPTIC TAGGING AND CAPTURE;

ACETYLCYSTEINE; ANIMALS; ANISOMYCIN; BEHAVIOR, ANIMAL; CALCIUM CHANNEL BLOCKERS; CONDITIONING, CLASSICAL; EXCITATORY AMINO ACID ANTAGONISTS; FEAR; HIPPOCAMPUS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASE INHIBITORS; RATS; SIROLIMUS; UBIQUITIN;

EID: 84896944611     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400423111     Document Type: Article

References (49)

1. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385(6616):533-536. (Pubitemid 27074671)
2. Frey U, Morris RG (1998) Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21(5):181-188. (Pubitemid 28191809)
3. Uzakov S, Frey JU, Korz V (2005) Reinforcement of rat hippocampal LTP by holeboard training. Learn Mem 12(2):165-171. (Pubitemid 40517084)
4. Almaguer-Melian W, Bergado JA, Martínez-Martí L, Duany-Machado C, Frey JU (2010) Basolateral amygdala stimulation does not recruit LTP at depotentiated synapses. Physiol Behav 101(4):549-553.
5. Moncada D, Ballarini F, Martinez MC, Frey JU, Viola H (2011) Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation. Proc Natl Acad Sci USA 108(31):12931-12936.
6. Sajikumar S, Frey JU (2004) Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol Learn Mem 82(1):12-25. (Pubitemid 38737426)
7. Almaguer-Melian W, et al. (2012) Novelty exposure overcomes foot shock-induced spatial-memory impairment by processes of synaptic-tagging in rats. Proc Natl Acad Sci USA 109(3):953-958.
8. 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(4):831-851.
9. 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(28):7476-7481. (Pubitemid 47066574)
10. Ballarini F, Moncada D, Martinez MC, Alen N, Viola H (2009) Behavioral tagging is a general mechanism of long-term memory formation. Proc Natl Acad Sci USA 106(34):14599-14604.
11. Dalton GL, Wang YT, Floresco SB, Phillips AG (2008) Disruption of AMPA receptor endocytosis impairs the extinction, but not acquisition of learned fear. Neuropsychopharmacology 33(10):2416-2426.
12. Dalton GL, Wu DC, Wang YT, Floresco SB, Phillips AG (2012) NMDA GluN2A and GluN2B receptors play separate roles in the induction of LTP and LTD in the amygdala and in the acquisition and extinction of conditioned fear. Neuropharmacology 62(2):797-806.
13. de Carvalho Myskiw J, Benetti F, Izquierdo I (2013) Behavioral tagging of extinction learning. Proc Natl Acad Sci USA 110(3):1071-1076.
14. Pavlov IP, Anrep GV (1927) Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex (Oxford Univ Press, London).
15. Vianna MR, et al. (2000) Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem 7(5):333-340.
16. Thompson RF (2009) Habituation: A history. Neurobiol Learn Mem 92(2):127-134.
17. Myskiw JC, et al. (2008) On the participation of mTOR in recognition memory. Neurobiol Learn Mem 89(3):338-351. (Pubitemid 351318273)
18. Da Silva WC, Cardoso G, Bonini JS, Benetti F, Izquierdo I (2013) Memory reconsolidation and its maintenance depend on L-voltage-dependent calcium channels and CaMKII functions regulating protein turnover in the hippocampus. Proc Natl Acad Sci USA 110(16):6566-6570.
19. Fiorenza NG, Rosa J, Izquierdo I, Myskiw JC (2012) Modulation of the extinction of two different fear-motivated tasks in three distinct brain areas. Behav Brain Res 232(1):210-216.
20. Rosa J, Myskiw JC, Furini CR, Sapiras GG, Izquierdo I (2013) Fear extinction can be made state-dependent on peripheral epinephrine: Role of norepinephrine in the nucleus tractus solitarius. Neurobiol Learn Mem, 10.1016/j.nlm.2013.09.018.
21. Netto CA, et al. (1985) Response of the rat brain beta-endorphin system to novelty: Importance of the fornix connection. Behav Neural Biol 43(1):37-46. (Pubitemid 15139133)
22. Myhrer T (1988) Exploratory behavior and reaction to novelty in rats with hippocampal perforant path systems disrupted. Behav Neurosci 102(3):356-362.
23. Lopez-Salon M, et al. (2001) The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 14(11):1820-1826.
24. Liao CK, Jeng CJ, Wang HS, Wang SH, Wu JC (2013) Lipopolysaccharide induces degradation of connexin43 in rat astrocytes via the ubiquitin-proteasome proteolytic pathway. PLoS ONE 8(11):e79350.
25. Artinian J, et al. (2008) Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation. Eur J Neurosci 27(11):3009-3019. (Pubitemid 351832218)
26. Fonseca R, Vabulas RM, Hartl FU, Bonhoeffer T, Nägerl UV (2006) A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52(2):239-245. (Pubitemid 44548341)
27. Cai F, Frey JU, Sanna PP, Behnisch T (2010) Protein degradation by the proteasome is required for synaptic tagging and the heterosynaptic stabilization of hippocampal late-phase long-term potentiation. Neuroscience 169(4):1520-1526.
28. Osmulski PA, Gaczynska M (2013) Rapamycin allosterically inhibits the proteasome. Mol Pharmacol 84(1):104-113.
29. Seoane A, Massey PV, Keen H, Bashir ZI, Brown MW (2009) L-type voltage-dependent calcium channel antagonists impair perirhinal long-term recognition memory and plasticity processes. J Neurosci 29(30):9534-9544.
30. Perugini A, Laing M, Berretta N, Aicardi G, Bashir ZI (2012) Synaptic plasticity from amygdala to perirhinal cortex: A possible mechanism for emotional enhancement of visual recognition memory? Eur J Neurosci 36(4):2421-2427.
31. Sadanandappa MK, et al. (2013) Synapsin function in GABA-ergic interneurons is required for short-term olfactory habituation. J Neurosci 33(42):16576-16585.
32. Giese KP, Mizuno K (2013) The roles of protein kinases in learning and memory. Learn Mem 20(10):540-552.
33. Lucchesi W, Mizuno K, Giese KP (2011) Novel insights into CaMKII function and regulation during memory formation. Brain Res Bull 85(1-2):2-8.
34. Myskiw JC, Fiorenza NG, Izquierdo LA, Izquierdo I (2010) Molecular mechanisms in hippocampus and basolateral amygdala but not in parietal or cingulate cortex are involved in extinction of one-trial avoidance learning. Neurobiol Learn Mem 94(2):285-291.
35. Sajikumar S, Li Q, Abraham WC, Xiao ZC (2009) Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1. Learn Mem 16(3):178-186.
36. Redondo RL, et al. (2010) Synaptic tagging and capture: Differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30(14):4981-4989.
37. Tinsley CJ, et al. (2009) A role for calcium-calmodulin-dependent protein kinase II in the consolidation of visual object recognition memory. Eur J Neurosci 30(6):1128-1139.
38. Popkirov SG, Manahan-Vaughan D (2011) Involvement of the metabotropic glutamate receptor mGluR5 in NMDA receptor-dependent, learning-facilitated long-term depression in CA1 synapses. Cereb Cortex 21(3):501 -509.
39. 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. (Pubitemid 351451900)
40. Barros DM, et al. (2000) Molecular signalling pathways in the cerebral cortex are required for retrieval of one-trial avoidance learning in rats. Behav Brain Res 114(1-2):183-192.
41. Knapska E, et al. (2012) Functional anatomy of neural circuits regulating fear and extinction. Proc Natl Acad Sci USA 109(42):17093-17098.
42. Tsumoto T (1990) Long-term potentiation and depression in the cerebral neocortex. Jpn J Physiol 40(5):573-593.
43. Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: Ten years of progress. Annu Rev Psychol 63:129- 151.
44. Sanderson TM, Collingridge GL, Fitzjohn SM (2011) Differential trafficking of AMPA receptors following activation of NMDA receptors and mGluRs. Mol Brain 4:30.
45. Dickinson BA, et al. (2009) A novel mechanism of hippocampal LTD involving muscarinic receptor-triggered interactions between AMPARs, GRIP and liprin-alpha. Mol Brain 2:18.
46. Monfils MH, Cowansage KK, Klann E, LeDoux JE (2009) Extinction- reconsolidation boundaries: Key to persistent attenuation of fear memories. Science 324(5929):951-955.
47. Schiller D, Kanen JW, LeDoux JE, Monfils MH, Phelps EA (2013) Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement. Proc Natl Acad Sci USA 110(50):20040-20045.
48. Committee on Care and Use of Laboratory Animals (1985) Guide for the Care and Use of Laboratory Animals (National Institutes of Health, Bethesda), DHHS Publ No (NIH) 85-23.
49. Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates (Academic, Orlando, FL), 2nd Ed.