Modulation of the extinction of fear learning

Brain Research Bulletin

Volumn 105, Issue , 2014, Pages 61-69

  Myskiw, Jociane C ^a   Izquierdo, Ivan ^a   Furini, Cristiane R G ^a  

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

Author keywords

Behavioral tagging of extinction; Dopaminergic D1 receptors; Endocannabinoid receptors; Histamine H2 receptors; Noradrenergic receptors; State dependency of extinction

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 AMINO 5 PHOSPHONOVALERIC ACID; ADRENALIN; ANANDAMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID; CANNABINOID RECEPTOR; CATECHOLAMINE; CYCLOSERINE; DEXTRO SERINE; ETHYLAMINE; GLUCOCORTICOID; HISTAMINE; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCARINIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NORADRENALIN; PRAZOSIN; PROPRANOLOL; PROTEIN KINASE; RANITIDINE; TIMOLOL; CELL SURFACE RECEPTOR; SEX HORMONE;

BASOLATERAL AMYGDALA; BRAIN CORTEX; CHOLINERGIC STIMULATION; CONDITIONING; ENZYME PHOSPHORYLATION; EPIGENETICS; FEAR; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HUMAN; INSULA; MEMORY; MEMORY CONSOLIDATION; MONOSYNAPTIC REFLEX; NEOCORTEX; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REINFORCEMENT; REVIEW; RNA SYNTHESIS; SPATIAL MEMORY; TASTE AVERSION; VENTROMEDIAL PREFRONTAL CORTEX; ANIMAL; BRAIN; LEARNING; METABOLISM; PHYSIOLOGY;

ANIMALS; BRAIN; FEAR; GONADAL STEROID HORMONES; HUMANS; LEARNING; RECEPTORS, CELL SURFACE; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84901492296     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2014.04.006     Document Type: Review

References (141)

1. Abarbanel H., Huerta R., Rabinovich M.I. Dynamical model of long-term synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:10132-10137.
2. Almaguer-Melián W., Bergado-Rosado J., Pavón-Fuentes N., Alberti-Amador E., Mercerón-Martínez D., Frey J.U. Novelty exposure overcomes foot shock-induced spatial-memory impairment by processes of synaptic-tagging in rats. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:953-958.
3. Alonso M., Bekinschtein P., Cammarota M., Vianna M.R., Izquierdo I., Medina J.H. Endogenous BDNF is required for long-term memory formation in the rat parietal cortex. Learn. Mem. 2005, 12:504-510.
4. Amir A., Amano T., Paré D. Physiological identification and infralimbic responsiveness of rat intercalated amygdala neurons. J. Neurophysiol. 2011, 105:3054-3066.
5. Ashton J.C., Smith P.F., Darlington C.L. The effect of delta 9-tetrahydrocannabinol on the extinction of an adverse associative memory. Pharmacology 2008, 81:18-20.
6. Atsak P., Roozendaal B., Campolongo P. Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences. Neuroscience 2012, 204:104-116.
7. Azad S.C., Eder M., Simon W., Hapfelmeier G., Dodt H.U., Zieglgänsberger W., Rammes G. The potassium channel modulator flupirtine shifts the frequency-response function of hippocampal synapses to favour LTD in mice. Neurosci. Lett. 2004, 370:186-190.
8. Azad S.C., Kurz J., Marsicano G., Lutz B., Zieglgänsberger W., Rammes G. Activation of CB1 specifically located on GABAergic interneurons inhibits LTD in the lateral amygdala. Learn. Mem. 2008, 15:143-152.
9. Ballarini F., Moncada D., Martinez M.C., Alen N., Viola H. Behavioral tagging is a general mechanism of long-term memory formation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14599-14604.
10. Barco A., López de Armentía M., Alarcón J.M. Synapse-specific stabilization of plasticity processes: the synaptic tagging and capture hypothesis revisited 10 years later. Neurosci. Biobehav. Rev. 2008, 32:831-851.
11. Benetti F., Baldi E., Bucherelli C., Blandina P., Passani M.B. Histaminergic ligands injected into the nucleus basalis magnocellularis differentially affect fear conditioning consolidation. Int. J. Neuropsychopharmacol. 2013, 16:575-582.
12. Benetti F., Izquierdo I. Histamine infused into basolateral amygdala enhances memory consolidation of inhibitory avoidance. Int. J. Neuropsychopharmacol. 2013, 16:1539-1545.
13. Beninger R.J., Nakonechny P.L. Dopamine D1-like receptors and molecular mechanisms of incentive learning. Dopamine Disease States, 1996, 407-431. Fundación Cerebro y Mente, Madrid. R.J. Beninger, T. Palomo, T. Archer (Eds.).
14. Berlau D.J., McGaugh J.L. Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol. Learn. Mem. 2006, 86:123-132.
15. Berman D.E., Dudai Y. Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 2001, 291:2417-3249.
16. Bernabeu R., Bevilaqua L., Ardenghi P., Bromberg E., Schmitz P., Bianchin M., Izquierdo I., Medina J.H. Involvement of hippocampal D1/D5 receptor - cAMP signaling pathways in a late memory consolidation phase of an aversively-motivated task in rats. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:7041-7046.
17. Bernardi R.E., Lattal K.M. A role for alpha-adrenergic receptors in extinction of conditioned fear and cocaine conditioned place preference. Behav. Neurosci. 2010, 124:204-210.
18. Bevilaqua L.R., Bonini J.S., Rossato J.I., Izquierdo L.A., Cammarota M., Izquierdo I. The entorhinal cortex plays a role in extinction. Neurobiol. Learn. Mem. 2006, 85:192-197.
19. Blandina P., Munari L., Provensi G., Passani M.B. Histamine neurons in the tuberomamillary nucleus: a whole center or distinct subpopulations?. Front. Syst. Neurosci. 2012, 6:33.
20. Bonini J.S., Da Silva W.C., Da Silveira C.K., Köhler C.A., Izquierdo I., Cammarota M. Histamine facilitates consolidation of fear extinction. Int. J. Neuropsychopharmacol. 2011, 14:1209-1217.
21. Bouton M.E. Context and behavioral processes in extinction. Learn. Mem. 2004, 11:485-494.
22. Bouton M.E., Ricker S.T. Renewal of extinguished responding in a second context. Anim. Learn. Behav. 1994, 22:317-324.
23. Burgos-Robles A., Vidal-Gonzalez I., Santini E., Quirk G.J. Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 2007, 53:871-880.
24. Cho J.H., Deisseroth K., Bolshakov V.Y. Synaptic encoding of fear extinction in mPFC-amygdala circuits. Neuron 2013, 80(6):1491-1507.
25. Clarke J.R., Cammarota M., Gruart A., Izquierdo I., Delgado-Garcia J.M. Plastic modifications induced by object recognition memory processing. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:2652-2657.
26. Dalton G.L., Wang Y.T., Floresco S.B., Phillips A.G. Disruption of AMPA receptor endocytosis impairs the extinction, but not acquisition of learned fear. Neuropsychopharmacology 2008, 33:2416-2426.
27. Dalton G.L., Wu D.C., Wang Y.T., Floresco S.B., Phillips A.G. 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 2012, 62:797-806.
28. Das R.K., Kamboj S.K., Ramadas M., Yogan K., Gupta V., Redman E., Curran H.V., Morgan C.J. Cannabidiol enhances consolidation of explicit fear extinction in humans. Psychopharmacology 2013, 226:781-792.
29. Davis M. NMDA receptors and fear extinction: implications for cognitive behavioral therapy. Dialogues Clin. Neurosci. 2011, 13:463-474.
30. Debiec J., Bush D.E., LeDoux J.E. Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats-a possible mechanism for the persistence of traumatic memories in PTSD. Depress. Anxiety 2011, 28:186-193.
31. Do Monte F.H., Souza R.R., Bitencourt R.M., Kroon J.A., Takahashi R.N. Infusion of cannabidiol into infralimbic cortex facilitates fear extinction via CB1 receptors. Behav. Brain Res. 2013, 250:23-27.
32. Fiorenza N.G., Rosa J., Izquierdo I., Myskiw J.C. Modulation of the extinction of two different fear-motivated tasks in three distinct brain areas. Behav. Brain Res. 2012, 232:210-216.
33. Frey S., Frey J.U. Synaptic tagging and cross-tagging and related associative reinforcement processes of functional plasticity as the cellular basis for memory formation. Prog. Brain Res. 2008, 169:117-143.
34. Frey U., Morris R.G. Synaptic tagging and long-term potentiation. Nature 1997, 385:533-536.
35. Garcia-Delatorre P., Rodríguez-Ortiz C.J., Balderas I., Bermúdez-Rattoni F. Differential participation of temporal structures in the consolidation and reconsolidation of taste aversion extinction. Eur. J. Neurosci. 2010, 32:1018-1023.
36. Gomes G.M., Mello C.F., da Rosa M.M., Bochi G.V., Ferreira J., Barron S., Rubin M.A. Polyaminergic agents modulate contextual fear extinction in rats. Neurobiol. Learn. Mem. 2010, 93:589-595.
37. Green J.D. The hippocampus. Physiol. Rev. 1964, 44:561-608.
38. Gruart A., Muñoz M.D., Delgado-Garcia J.M. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J. Neurosci. 2006, 26:1087-1097.
39. Haubensak W., Kunwar P.S., Cai H., Ciocchi S., Wall N.R., Ponnusamy R., Biag J., Dong H.W., Deisseroth K., Callaway E.M., Fanselow M.S., Lüthi A., Anderson D.J. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 2010, 468:270-276.
40. Henneberger C., Papouin T., Oliet S.H., Rusakov D.A. Long-term potentiation depends on release of d-serine from astrocytes. Nature 2010, 463:232-236.
41. Holmes A., Quirk G.J. Pharmacological facilitation of fear extinction and the search for adjunct treatments for anxiety disorders-the case of yohimbine. Trends Pharmacol. Sci. 2010, 31:2-7.
42. Hölter S.M., Kallnik M., Wurst W., Marsicano G., Lutz B., Wojtak C.T. Cannabinoid CB1 receptor is dispensable for memory extinction in an appetitively-motivated learning task. Eur. J. Pharmacol. 2005, 510:69-74.
43. Igaz L.M., Vianna M.R., Medina J.H., Izquierdo I. Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning. J. Neurosci. 2002, 22:6781-6789.
44. Izquierdo I. Endogenous state dependence: memory depends on the relation between the neurohumoral and hormonal states present after training and at the time of testing. Neurobiology of Learning and Memory 1984, 333-350. Guilford Press, New York. G. Lynch, J.L. McGaugh, N.M. Weinberger (Eds.).
45. Izquierdo I., Bevilaqua J.R.M., Rossato J.I., Bonini J.S., Medina J.H., Cammarota M. Different molecular cascades in different sites of the brain control consolidation. Trends Neurosci. 2006, 29:496-505.
46. Izquierdo I., Dias R.D. Memory as a state dependent phenomenon: role of ACTH and epinephrine. Behav. Neural Biol. 1983, 38:144-151.
47. Izquierdo I., Medina J.H. Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol. Learn. Mem. 1995, 63:19-32.
48. Izquierdo I., Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 1997, 68:285-316.
49. Izquierdo I., Myskiw J.C. Brain interactions between processes triggered by memory retrieval and their use in the treatment of fear memory. Future Neurol. 2011, 6:307-309.
50. Izquierdo I., Netto C.A. The role of beta-endorphin in memory regulation. Ann. N.Y. Acad. Sci. 1985, 444:162-167.
51. Izquierdo I., Wyrwicka W., Sierra G., Segundo J.P. Establishment of a trace reflex during natural sleep of cats. Actual Neurophysiol. (Paris) 1965, 6:277-296.
52. Kandel E.R., Squire L.R. Neuroscience: breaking down scientific barriers to the study of brain and mind. Science 2000, 290:1113-1120.
53. Kerbage H., Richa S. Non-antidepressant long-term treatment in post-traumatic stress disorder (PTSD). Curr. Clin. Pharmacol. 2013, (Epub ahead of print February 4).
54. Klyubin I., Ondrejcak T., Hayes J., Vullen W.K., Mably A.J., Walsh D.M., Rowan M.J. Neurotransmitter receptor and time-dependence of the synaptic plasticity disrupting actions of Alzheimer' disease Aß in vivo. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2013, 369. 20130147, doi:10.1098/rtsb.2013.0147.
55. Kombian S.B., Malenka R.C. Simultaneous LTPof non-NMA- and LTD of NMA-receptor-mediated responses in the nucleus accumbens. Nature 1994, 368:242-246.
56. Komulainen P., Pedersen M., Hänninen T., Buunsgaard H., Lakka T.A., Kivipelto M., Hassinen M., Rauramaa T.H., Pedersen B.K., Rauramaa R. BDNF is a novel marker of cognitive function in ageing women: the DR' EXTRA study. Neurobiol. Learn. Mem. 2008, 90:596-603.
57. Konorski J. Conditioned Reflexes and Neuron Organization 1948, Cambridge University Press, Cambridge.
58. Lattal K.M., Wood M.A. Epigenetics and persistent memory: implications for reconsolidation and silent extinction beyond the zero. Nat. Neurosci. 2013, 16:124-129.
59. Ledgerwood L., Richardson R., Cranney J. d-Cycloserine facilitates extinction of learned fear: effects on reacquisition and generalized extinction. Biol. Psychiatry 2005, 57:841-847.
60. Li G., Nair S.S., Quirk G.J. A biologically realistic network model of acquisition and extinction of conditioned fear associations in lateral amygdala neurons. J. Neurophysiol. 2009, 101:1629-1646.
61. Lipp H.P., Schwegler H., Heimrich B., Cerbone A., Sadile A.G. Strain-specific correlations between hippocampal structural traits and habituation in a spatial novelty situation. Behav. Brain Res. 1987, 24:111-123.
62. Lu H., Park H., Poo M.M. Spike-timing-dependent BDNF secretion and synaptic plasticity. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2013, 369:20130132.
63. McGaugh J.L. Drug facilitation of learning and memory. Annu. Rev. Pharmacol. 1973, 13:229-241.
64. McGaugh J.L. Memory-a century of consolidation. Science 2000, 287:248-251.
65. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 2004, 27:1-28.
66. McGaugh J.L. Making lasting memories: remembering the significant. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:10402-10407.
67. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
68. Maren S. Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 2011, 70:830-845.
69. Maren S. Fear of the unexpected: hippocampus mediates novelty-induced return of extinguished fear in rats. Neurobiol. Learn. Mem. 2013, pii:S1074-7427(13)00096-8 (Epub ahead of print).
70. Marsicano G., Lafenêtre P. Roles of the endocannabinoid system in learning and memory. Curr. Top. Behav. Neurosci. 2009, 1:201-230.
71. Marsicano G., Lutz B. Neuromodulatory functions of the endocannabinoid system. J. Endocrinol. Invest. 2006, 29(Suppl. 3):27-46.
72. Marsicano G., Wojtak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., Hermann H., Tang J., Hofmann C., Zieglgänsberger W., Di Marzo V., Lutz B. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002, 418:530-534.
73. Mello-Carpes P.B., Izquierdo I. The nucleus of the solitary tract?nucleus paragigantocellularis?locus coeruleus?CA1 region of dorsal hippocampus pathway is important for consolidation of object recognition memory. Neurobiol. Learn. Mem. 2013, 100:56-63.
74. Milad M.R., Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002, 420:70-74.
75. Milad M.R., Quirk G.J. Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 2012, 63:129-151.
76. Milad M.R., Wright C.I., Orr S.P., Pitman R.K., Quirk G.J., Rauch S.L. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Psychiatry 2007, 62:446-454.
77. 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. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12931-12936.
78. Mueller D., Bravo-Rivera C., Quirk G.J. Infralimbic D2 receptors are necessary for fear extinction and extinction-related tone responses. Biol. Psychiatry 2010, 68:1055-1060.
79. Mueller D., Olivera-Figueroa L.A., Pine D.S., Quirk G.J. The effects of yohimbine and amphetamine on fear expression and extinction in rats. Psychopharmacology (Berl) 2009, 204:599-606.
80. Mueller D., Porter J.T., Quirk G.J. Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J. Neurosci. 2008, 28:369-375.
81. 3 receptor antagonist/inverse agonist ABT-239 enhances acetylcholine and histamine release and increases c-Fos expression. Neuropharmacology 2013, 70:131-140.
82. Myhrer T. Exploratory behavior and reaction to novelty in rats with hippocampal perforant path systems disrupted. Behav. Neurosci. 1988, 102:356-362.
83. Myskiw J.C., Furini C.R.G., Izquierdo I. Modulation of the extinction of fear learning. Psychology of Fear 2013, 83-95. Nova Science Publishers, New York. M.N. Purcella (Ed.).
84. Myskiw J.C., Benetti F., Izquierdo I. Behavioral tagging of extinction learning. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:1071-1076.
85. Myskiw J.C., Rossato J.I., Bevilaqua L.R., Medina J.H., Izquierdo I., Cammarota M. On the participation of mTOR in recognition memory. Neurobiol. Learn. Mem. 2008, 89:338-351.
86. Nader K. Memory traces unbound. Trends Neurosci. 2003, 26:65-72.
87. Netto C.A., Cavalheiro E.A., Carrasco M.A., Volkmer N., Dias R.D., Izquierdo I. Response of the rat brain beta-endorphin system to novelty: importance of the fornix connection. Behav. Neural Biol. 1985, 43:37-46.
88. Overton D.A. Basic mechanisms of state-dependent learning. Psychopharmacol. Bull. 1978, 14:67-68.
89. Otani S., Daniel H., Takita M., Crépel F. Long-term depression induced by postsynaptic group II metabotropic glutamate receptors linked to phospholipase C and intracellular calcium rises in rat pre-frontal cortex. J. Neurosci. 2002, 22:3434-3444.
90. Pape H.C., Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev. 2010, 90:419-463.
91. Pape H.C., Narayanan R.T., Smid J., Stork O., Seidenbecher T. Theta activity in neurons and networks of the amygdala related to long-term fear memory. Hippocampus 2005, 15:874-880.
92. Passani M.B., Blandina P. Histamine receptors in the CNS as targets for therapeutic intervention. Trends Pharmacol. Sci. 2011, 32:242-249.
93. Pavlov I.P. Conditioned Reflexes 1927, Oxford University Press, London.
94. Penfield W., Milner B. Memory deficit produced by bilateral lesions in the hippocampal zone. AMA Arch. Neurol. Psychiatry 1958, 79:475-497.
95. Peters J., Dieppa-Perea L.M., Melendez L.M., Quirk G.J. Induction of fear extinction with hippocampal-infralimbic BDNF. Science 2010, 328:1288-1290.
96. Phelps E.A., Delgado M.R., Nearing K.I., LeDoux J.E. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 2004, 43:897-905.
97. Pluchino N., Russo M., Santoro A.N., Litta P., Cela V., Genazzani A.R. Steroid hormones and BDNF. Neuroscience 2013, 239:271-279.
98. Porte Y., Trifilieff P., Wolff M., Micheau J., Buhot M.C., Mons N. Extinction of spatial memory alters CREB phosphorylation in hippocampal CA1. Hippocampus 2011, 21:1169-1179.
99. Potter W.B., Basu T., O'Riordan K.J., Kirchner A., Rutecki P., Burger C., Roopra A. Reduced juvenile long-term depression in tuberous sclerosis complex is mitigated in adults by compensatory recruitment of mGluR5 and Erk signaling. PLoS Biol. 2013, 11(8):e1001627.
100. Quirk G.J. Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery. Learn. Mem. 2002, 9:402-407.
101. Rabinak C.A., Angstadt M., Lyons M., Mori S., Milad M.R., Liberzon I., Luan Phan K. Cannabinoid modulation of prefrontal-limbic activation during fear extinction learning and recall in humans. Neurobiol. Learn. Mem. 2013, pii:S1074-7427(13)00186-X [Epub ahead of print 2013, September 19].
102. Rabinak C.A., Phan K.L. Cannabinoid modulation of fear extinction brain circuits: a novel target to advance anxiety treatment. Curr. Pharm. Des. 2013, (Epub ahead of print).
103. Ramot A., Akirav I. Cannabinoid receptors activation and glucocorticoid receptors deactivation in the amygdala prevent the stress-induced enhancement of a negative learning experience. Neurobiol. Learn. Mem. 2012, 97:393-401.
104. Rescorla R.A. Retraining of extinguished Pavlovian stimuli. J. Exp. Psychol.: Anim. Behav. Process. 2001, 27:115-124.
105. Rescorla R.A. Spontaneous recovery. Learn. Mem.ry 2004, 11:501-509.
106. Rosa J., Myskiw J.C., Furini C.R., Sapiras G.G., Izquierdo I. Fear extinction can be made state-dependent on peripheral epinephrine: role of norepinephrine in the nucleus tractus solitarius. Neurobiol. Learn. Mem. 2013, pii:S1074-7427(13)00195-0 (Epub ahead of print).
107. Roozendaal B., de Quervain D.J., Ferry B., Setlow B., McGaugh J.L. Basolateral amygdala-nucleus accumbens interactions in mediating glucocorticoid enhancement of memory consolidation. J. Neurosci. 2001, 21:2518-2525.
108. Roozendaal B., McGaugh J.L. Memory modulation. Behav. Neurosci. 2011, 125:797-824.
109. Rudenko A., Dawlaty M.M., Seo J., Cheng A.W., Meng J., Le T., Faull K.F., Jaenisch R., Tsai L.H. Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 2013, 79:1109-1122.
110. Rush A.M., Wu J., Rowan M.J., Anwyl R. Group I metabotropic glutamate receltor (mGluR)-dependent long-term depression mediated via p38 mitogen-activated protein kinase is inhibited by previous high-frequency stimulation and activationof mGluRs and protein kinase C in the rat dentate gyrus in vitro. J. Neurosci. 2002, 22:6121-6128.
111. Saito Y., Matsumoto M., Yanagawa Y., Hiraide S., Inoue S., Kubo Y., Shimamura K., Togashi H. Facilitation of fear extinction by the 5-HT(1A) receptor agonist tandospirone: possible involvement of dopaminergic modulation. Synapse 2013, 67:161-170.
112. Sakata K., Martinowich K., Woo N.H., Schloesser R.J., Jimenez D.V., Ji Y., Shen L., Lu B. Role of activity-dependent BDNF expression in hippocampal-prefrontal cortical regulation of behavioral perseverance. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:15103-15108.
113. Santini E., Muller R.U., Quirk G.J. Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J. Neurosci. 2001, 21:9009-9017.
114. Santini E., Quirk G.J., Porter J.T. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J. Neurosci. 2008, 28:4028-4036.
115. Santini E., Sepúlveda-Orengo M., Porter J.T. Muscarinic receptors modulate the intrinsic excitability of infralimbic neurons and consolidation of fear extinction. Neuropsychopharmacology 2012, 37:2047-2056.
116. Sarabdjitsingh R.A., Kofink D., Karst H., de Kloet E.R., Joëls M. Stress-induced enhancement of mouse amygdalar synaptic plasticity depends on glucocorticoid and ß-adrenergic activity. PLoS One 2012, 7:e42143.
117. Saunders R.C., Rosene D.L., Van Hoesen G.W. Comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: II. Reciprocal and non-reciprocal connections. J. Comp. Neurol. 1988, 271:185-207.
118. Schiller D., Monfils M.H., Raio C.M., Johnson D.C., LeDoux J.E., Phelps E.A. Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 2010, 463:49-53.
119. Schwabe L., Joëls M., Roozendaal B., Wolf O.T., Oitzl M.S. Stress effects on memory: an update and integration. Neurosci. Biobehav. Rev. 2012, 36:1740-1749.
120. Senn V., Wolff S.B., Herry C., Grenier F., Ehrlich I., Gründemann J., Fadok J.P., Müller C., Letzkus J.J., Lüthi A. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 2014, 81:428-437.
121. Setlow B., Roozendaal B., McGaugh J.L. Involvement of a basolateral amygdala complex-nucleus accumbens pathway in glucocorticoid-induced modulation of memory consolidation. Eur. J. Neurosci. 2000, 12:367-375.
122. Sotres-Bayon F., Sierra-Mercado D., Pardilla-Delgado E., Quirk G.J. Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 2012, 76:804-812.
123. Squire L.R. The legacy of patient H.M. for neuroscience. Neuron 2009, 61:6-9.
124. Stafford J.M., Lattal K.M. Is an epigenetic switch the key to persistent extinction?. Neurobiol. Learn. Mem. 2011, 96:35-40.
125. Stafford J.M., Maugham D.K., Ilioi E.C., Lattal K.M. Exposure to a fearful context during periods of memory plasticity impairs extinction via hyperactivation of frontal-amygdalar circuits. Learn. Mem. 2013, 20:156-163.
126. Szapiro G., Galante J.M., Barros D.M., Levi de Stein M., Vianna M.R., Izquierdo L.A., Izquierdo I., Medina J.H. Molecular mechanisms of memory retrieval. Neurochem. Res. 2002, 27:1491-1498.
127. Szapiro G., Vianna M.R., McGaugh J.L., Medina J.H., Izquierdo I. The role of NMDA glutamate receptors, PKA, MAPK, and CaMKII in the hippocampus in extinction of conditioned fear. Hippocampus 2003, 13:53-58.
128. Thanellou A., Green J.T. Spontaneous recovery but not reinstatement of the extinguished conditioned eyeblink response in the rat. Behav. Neurosci. 2011, 125:613-625.
129. Tronson N.C., Schrick C., Guzman Y.F., Huh K.H., Srivastava D.P., Penzes P., Guedea A.L., Gao C., Radulovic J. Segregated populations of hippocampal principal CA1 neurons mediating conditioning and extinction of contextual fear. J. Neurosci. 2009, 29:3387-3394.
130. Tsumoto T. Long-term potentiation and depression in the cerebral neocortex. Jpn. J. Physiol. 1990, 40:573-593.
131. Van Hoesen G.W. Neural systems of the non-human primate forebrain implicated in memory. Ann. N.Y. Acad. Sci. 1985, 444:97-112.
132. Vianna M.R., Coitinho A.S., Izquierdo I. Role of the hippocampus and amygdala in the extinction of fear-motivated learning. Curr. Neurovasc. Res. 2004, 1:55-60.
133. Vianna M.R., Szapiro G., McGaugh J.L., Medina J.H., Izquierdo I. Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus. Proc. Natl. Acad. Sci. 2001, 98:12251-12254.
134. Whitlock J.R., Heynen A.J., Shuler M.G., Bear M.G. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
135. Wichmann R., Fornari R.V., Roozendaal B. Glucocorticoids interact with the noradrenergic arousal system in the nucleus accumbens shell to enhance memory consolidation of both appetitive and aversive taste learning. Neurobiol. Learn. Mem. 2012, 98:197-205.
136. Williams C.L., McGaugh J.L. Reversible inactivation of the nucleus of the solitary tract impairs retention performance in an inhibitory avoidance task. Behav. Neural Biol. 1992, 58:204-210.
137. Williams C.L., McGaugh J.L. Reversible lesions of the nucleus of the solitary tract attenuate the memory-modulating effects of posttraining epinephrine. Behav. Neural Biol. 1993, 107:955-962.
138. Wojtak C.T. Role of endogenous cannabinoids in cognition and emotionality. Mini Rev. Med. Chem. 2005, 5:659-670.
139. Yin J.C., Wallach J.S., Del Vecchio M., Wilder E.L., Zhou H., Quinn W.G., Tully T. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 1994, 79:49-58.
140. Zornetzer S.F. Neurotransmitter modulation and memory. A new neuropharmacological phrenology?. Psychopharmacology: A Generation of Progress 1978, 597. Raven Press, New York. M.A. Lipton, A. DiMascio, K.F. Killam (Eds.).
141. Zovkic I.B., Meadows J.P., Kaas G.A., Sweatt J.D. Interindividual variability in stress susceptibility: a role for epigenetic mechanisms in PTSD. Front. Psychiatry 2013, 4:60.