Extinction learning: Neurological features, therapeutic applications and the effect of aging

Future Neurology

Volumn 3, Issue 2, 2008, Pages 133-140

  Izquierdo, Ivan ^a   Bevilaqua, Lia R M ^a   Lima, Ramón H ^a   Clarke, Julia R ^a   da Costa, Jaderson Costa ^a   Cammarota, Martín ^a  

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

Author keywords

Extinction learning; Learned fear syndromes; Molecular basis; Phobias; Post traumatic stress disorder; Systems; Treatment

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; ANISOMYCIN; CANNABINOID 1 RECEPTOR; CANNABINOID DERIVATIVE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOSERINE; DESIPRAMINE; DIZOCILPINE; FLUOXETINE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE (CALCIUM,CALMODULIN) II;

AGING; AMYGDALOID NUCLEUS; ANXIETY DISORDER; CINGULATE GYRUS; CLINICAL TRIAL; CORRELATION ANALYSIS; DRUG EFFICACY; DRUG POTENTIATION; ENTORHINAL CORTEX; HIPPOCAMPUS; HUMAN; INFORMATION RETRIEVAL; LONG TERM MEMORY; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; MOLECULAR MECHANICS; NONHUMAN; ORBITAL CORTEX; PHOBIA; POSTTRAUMATIC STRESS DISORDER; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; REINFORCEMENT; REVIEW; TREATMENT RESPONSE;

EID: 40749091249     PISSN: 14796708     EISSN: None     Source Type: Journal    
DOI: 10.2217/14796708.3.2.133     Document Type: Review

References (92)

1. Pavlov IP: Conditioned Reflexes. Oxford University Press, London, UK (1927).
2. Rescorla RA. Retraining of extinguished Pavlovian stimuli. J. Exp. Psychol. Anim. Behav. Process 27, 115-124 (2001).
3. Cammarota M, Bevilaqua LRM, Kerr DH, Medina JH, Izquierdo I: Inhibition of mRNA and protein synthesis in the CA1 region of the dorsal hippocampus blocks reinstallment of an extinguished conditioned fear response. J. Neurosci. 23, 737-741 (2003).
4. Konorski J: Conditioned Reflexes and Neuron Organization. Cambridge University Press, Cambridge, UK (1949).
5. Vianna MRM, Szapiro G, McGaugh JL, Medina JH, Izquierdo I: Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus. Proc. Natl Acad. Sci. USA 94, 11251-11254 (2001).
6. Izquierdo I, Wyrwicka W, Sierra G, Segundo JP: Établissement de reflexes conditionnés de trace pendant le sommeil naturel chez le chat. Actual Neurophysiol. 6, 277-296 (1965).
7. Davis M, Ressler K, Rothman BO, Richardson R. Effects of D-cycloserine on extinction: translation from preclinical to clinical work. Biol. Psychiat. 60, 369-375 (2006).
8. Beckett WS: Post-traumatic stress disorder. N. Engl. J. Med. 346, 1495-1498 (2002).
9. Rothbaum BO, Davis M: Applying learning principles to the treatment of post-trauma reactions. Ann. NY Acad. Sci. 1008, 112-121 (2003).
10. Hoffmann SG: Enhanced exposure-based therpy from a translational research perspective. Behav. Res. Ther. 45, 1987-2001 (2007).
11. Freud S: Obsession and phobias. In: The Standard Edition of the Complete Psychological Works of Sigmund Freud. Hogarth Press, London, UK 3, 74-100 (1962).
12. Hytten K, Herlofsen P: Accident simulation as a new therapy technique for post-traumatic stress disorder. A case study. Acta Pychiatr. Scand. Suppl. 355, 79-83 (1989).
13. Vaughan K, Tarrier N: The use of image habituation training with post-traumatic stress disorders. Br. J. Psychiatry 161, 658-664 (1992).
14. Myers KM, Davis M: Behavioral and neural analysis of extinction. Neuron 36, 567-584 (2002).
15. Myers KM, Davis M: Mechanisms of fear extinction. Mol. Pychiat. 12, 120-150 (2007).
16. Quirk GJ, Mueller D: Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33, 56-72 (2008).
17. Quirk GJ: Extinction: new excitement for an old phenomenon. Biol. Psychiatry 60, 317-318 (2006).
18. Szapiro G, Vianna MRM, McGaugh JL, Medina JH, Izquierdo I: The role of NMDA glutamate receptors, PKA, MAPK, and CaMKII in the hippocampus in extinction of conditioned fear. Hippocampus 13, 53-58 (2003).
19. Vianna MRM, Coitinho AS, Izquierdo I: Role of the hippocampus and amygdala in the extinction of fear-motivated learning. Curr. Neurovasc. Res. 1, 55-60 (2004).
20. Bahar A, Samuel A, Hazvi S, Dudai Y: The amygdalar circuit that acquires taste aversion memory differs fiom the circuit that extinguishes it. Eur. J. Neurosci. 17, 1527-1530 (2003).
21. Lu KT, Walker DL, Davis M: Mitogen protein kinase cascade in the basolateral nucleus of the amygdala is involved in extinction of fear-potentiated startle. J. Neurosci 21, RC162 (2003).
22. Walker DL, Ressler KJ, Lu KT, Davis M: Facilitation of conditioned fear extinction by systemic administration or intra-amygdala infusions of D-cycloserine as assessed by fear-potentiated startle in rats. J. Neurosci. 22, 2343-2351 (2002).
23. Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ: Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 53, 871-880 (2007).
24. Quirk GJ: Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery. Learn. Mem. 9, 402-407 (2002).
25. Quirk GJ, Beer JS: Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr. Opin. Neurobiol. 16, 723-727 (2006).
26. Bevilaqua LRM, Bonini JS, Rossato JI, Izquierdo LA, Cammarota M, Izquierdo I: The entorhinal cortex plays a role in extinction. Neurobiol. Learn. Mem. 86, 192-197 (2006).
27. Berman DE, Dudai Y: Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 291, 2417-2419 (2001).
28. Cammarota M, Bevilaqua LRM, Rossato JI, Ramirez MA, Medina JH, Izquierdo I: Relationship between short- and long-term memory and short- and long-term extinction. Neurobiol. Learn. Mem. 84, 25-32 (2006).
29. Phelps EA, Delgado MR, Nearing KI, LeDoux JE: Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43, 897-905 (2004).
30. Akirav I, Maroon M: Ventromedial prefrontal cortex is obligatory for consolidation and reconsolidation of object recognition memory. Cerebral Cortex 16, 1759-1765 (2006).
31. Akirav I, Maroun M: The role of the medial prefrontal cortex-amygdala circuit in stress effects of the extinction of fear. Neural Plast. 30873 (2007)
32. Milad MR. Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL: Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Pychiatry 62(5), 446-454 (2007).
33. Kalisch R, Korenfeld E, Sterphan KE, Weiskopf N, Seymour B, Dolan, RJ: Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J. Neurosci. 26, 9503-9511
34. Milad MR, Quirk GJ: Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 26, 70-74 (2002).
35. Santini E, Ge H, Ren K, Pena de Ortiz S, Quirk GJ: Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J. Neurosci. 24, 5704-5710 (2004).
36. Akirav I, Raizel H, Maroun M: Enhancement of conditioned fear extinction by infusion of the GABA agonist muscimol into the rat prefrontal cortex and amygdala. Eur. J. Neurosci. 23, 758-764 (2006).
37. Izquierdo LA, Barros DM, da Costa JC et al.: A link between role of two prefrontal areas in immediate memory and in long-term memory consolidation. Neurobiol. Learn. Mem. 88, 160-188 (2007).
38. Blum S, Runyan JD, Dash PK: Inhibition of prefrontal protein synthesis following recall does not disrupt memory for trace fear conditioning. BMC Neurosci 7, 67-70 (2007).
39. Gauthier M, Destrade C: Late post-learning effect of entorhinal cortex electrical stimulation persists despite destruction of the perforant path. Brain Res. 310, 174-179 (1984).
40. Oniani TN, Nachkebia NG, Nachkebia AY, Chkhartishvili EV, Oniani LT: The influence of electrocoagulation of the septum and section of the entorhinal cortex on general behaviour and memory in cars. Acta Physiol Hung. 74, 9-25 (1989).
41. Ueki A, Miwa C, Miyoshi K: Impairment in the acquisition of passive and active avoidance learning tasks due to bilateral entorhinal cortex lesions. J. Neurol. Sci. 125, 14-21 (1994).
42. Freeman JH Jr, Weible A, Rossi J, Gabriel M: Lesions of the entorhinal cortex disrupt behavioral and neuronal responses to context change during extinction of discriminative avoidance behavior. Exp. Brain Res. 115, 445-457 (1997).
43. Hyman BT, Van Hoesen GW, Damasio AR: Memory-related neural systems in Alzheimer's disease: an anatomic study. Neurology 40, 1721-1730 (1990).
44. Van Hoesen GW: Neural systems of the non-human primate forebrain implicated in memory. Ann. NY Acad. Sci. 444, 97-112 (1985).
45. Milad MR, Quinn BT, Pitman RK, Orr SP, Fischl B, Rauch SL: Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proc. Natl Acad. Sci. USA 102, 10706-10711 (2005).
46. Rauch SL, Milad MR, Orr SP, Quinn BT, Fischl B, Pitman RK: Orbitofrontal thickness, retention of fear extinction, and extraversion. Neuroreport 16, 1909-1912 (2005).
47. Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL: A role of the human dorsal anterior cingulate cortex in fear expression. Biol. Psychiat. 62, 1191-1194 (2007).
48. Berlau DJ, McGaugh JL: Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol. Learn. Mem. 83, 123-132 (2006).
49. Izquierdo I, Bevilaqua LRM, Rossato JI, Bonini JS, Medina JH, Cammarota M: Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 29, 496-505 (2006).
50. Lin CH, Yeh SH, Lu HY, Gean PW: The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J. Neurosci. 23, 8310-8317.
51. Izquierdo I, Barros DM, Mello e Souza T, Souza MM, Izquierdo, JA, Medina JH: Mechanisms for memory types differ. Nature 393, 635-636 (1998).
52. Izquierdo I, Medina JH: GABAA receptor modulation of memory: the role of endogenous benzodiazepines. Trends Pharmacol. Sci. 12, 260-265 (1991).
53. Port RL, Seybold KS: Manipulation of NMDA-receptor activity alters extinction of an instrumental response in rats. Physiol. Behav. 64, 391-393 (1998).
54. Lee JL, Milton AL, Everitt BJ: Reconsolidation and extinction of conditioned fear: inhibition and potentiation. J. Neurosci. 26, 10051-10056 (2006).
55. Otto MW, Basden SL, Leyro, TM, McHugh RK, Hoffmann SG: Clinical perspectives on the combination of D-cycloserine and cognitive-behavioral therapy for the treatment of anxiety disorders. CNS Spectr. 12, 59-61 (2007).
56. Vervliet B: Learning and memory in conditioned fear extinction: effects of D-cycloserine. Acta Physiol. (Amst.) (2007) (Epub ahead of print).
57. Langton JH, Kim JH, Nicholas J, Richardson R: The effect of the NMDA receptor antagonist MK-801 on the acquisition and extinction of learned fear in the developing rat. Learn. Mem. 14, 665-668 (2007).
58. Sotres-Bayon F, Bush DE, LeDoux JE: Acquisition of fear extinction requires activation of NR2B-containing NMDA receptors in the lateral amygdala. Neuropsychopharmacol 32, 1929-1940 (2007).
59. Valenzuela-Harrington M, Gruart A, Delgado-García JM: Contribution of NMDA receptor NR2B subunit to synaptic plasticity during associative learning in behaving rats. Eur. J. Neurosci. 25(3), 830-836 (2007).
60. Shi R, Itagaki N, Sugawara I: Overview of anti-tuberculosis (TB) drugs and their resistance mechanisms. Mini Rev. Med. Chem. 7, 1177-1185(2007).
61. Marsicano G, Wotjak CT, Azad SC et al.: The endogenous cannabinoid system controls extinction of aversive memories. Nature 418(6897), 530 (2002).
62. Hölter SM, Kallnik M, Wurst W, Marsicano G, Lutz B, Wotjak CT: Cannabinoid CB1 receptor is dispensable for memory extinction in an appetitivelymotivated learning task. Eur. J. Pharmacol. 510, 69-74 (2005).
63. Kamprath K, Marsicano G, Tang J et al.: Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci. 26, 6677-6686 (2006).
64. Marsicano G, Lutz B: Neuromodulatory functions of the endocannabinoid system. J. Endocrinol. Invest. 29(Suppl. 3), 27-36 (2006).
65. Hansen HH, Krutz B, Sifringer M et al.: Cannabinoids enhance susceptibility of immature brain to ethanol neurotoxicity, Ann. Neurol. DOI: 10.1002/ana.21287 (2007).
66. Steiner MA, Marsicano G, Nestler EJ, Holsboer F, Lutz B, Wotjak CT: Antidepressant-like behavioral effects of impaired cannabinoid receptor type 1 signaling coincide with exaggerated corticosterone secretion in mice. Psychoneuroendocrinology. 33, 54-67 (2007).
67. Lafenetre P, Chaouloff F, Marsicano G: The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacol. Res. 56, 367-381 (2007).
68. Manzanares J, Urigüen L, Rubio G, Palomo T: Role of endocannabinoid system in mental diseases. Neurotox. Res. 6, 213-224 (2004).
69. Urigüen L, Pérez-Rial S, Ledent C, Palomo T, Manzanares J: Impaired action of anxiolytic drugs in mice deficient in cannabinoid CB1 receptors. Neuropharmacology 46, 966-973 (2004).
70. Huang H, Acuna-Goyrolea C, Li Y, Cheng HM, Obrietan K, van den Pol AN: Cannabinoids excite hypothalamic melanin-concentrating hormone but inhibit hypocretin/orexin neurons: implications for cannabinoid actions on food intake and cognitive arousal. J. Neurosci. 27, 4870-4871 (2007).
71. Hoffman AF, Oz M, Yang R, Lichtman AH, Lupica CR: Opposing actions of chronic A9-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation. Learn. Mem. 14, 63-74 (2007).
72. Azad SC, Eder M, Marsicano G, Lutz B, Zieglgänsberger W, Rammes G: Activation of the cannabinoid receptor type 1 decreases glutamatergic and GABAergic synaptic transmission in the lateral amygdala of the mouse. Learn. Mem. 10, 116-128 (2003).
73. Rea K. Roche M, Finn DP: Supraspinal modulation of pain by cannabinoids: the role of GABA and glutamate. Br. J. Pharmacol. 152, 633-648 (2007).
74. Izquierdo LA, Barros DM, Medina JH, Izquierdo I: Exposure to novelty enhances retrieval of very remote memory in rats. Neurobiol. Learn. Mem. 79, 51-58 (2003).
75. Barad M: Later developments: molecular keys to age-related memory impairment. Alzheimer Dis. Assoc. Disord. 17, 168-176 (2003).
76. Schneider-Rivas S, Paredes-Carbajal C, Mascher D et al.: Effects of testosterone and growth hormone on long-term retention and extinction of a passive avoidance response in young and aged rats. Int. J. Neurosci. 117, 1443-1456 (2007).
77. Schneider-Rivas S, Rivas-Arancibia S, Vázquez-Pereyra F, Várquez-Sandoval R, Borgonio-Pérez G: Modulation of long-term memory and extinction responses induced by growth hormone (GH) and growth hormone releasing hormone (GHRH) in rats. Life Sci. 56, PL433-PL441 (1995).
78. Topic B, Dere E, Schulz D et al.: Aged and adult rats compared in acquisition and extinction of escape from the water maze: focus on individual differences. Behav. Neurosci. 119, 127-144 (2005).
79. Oliveira-Silva IF, Pinto L, Pereira SR et al.: Age-related deficit in behavioural extinction is counteracted by long-term ethanol consumption: correlation between 5-HIAA/5HT ratio in dorsal raphe nucleus and cognitive parameters. Behav. Brain Res. 180, 226-234 (2007).
80. Pires RG, Pereira SR, Carvalho FM, Oliveira-Silva IF, Ferraz VP, Ribeiro AM: Correlation between phosphorylation level of a hippocampal 86kDa protein and extinction of a behaviour in a model of Wernicke-Korsakoff syndrome. Behav. Brain Res. 180, 102-106 (2007).
81. Schulz D, Topic B, De Souza Silva MA. Huston JP: Extinction-induced immobility in the water maze and its neurochemical concomitants in aged and adult rats: a possible model for depression? Neurobiol. Learn. Mem. 82, 128-141, (2004).
82. Schulz D, Buddenberg T, Huston JP: Extinction-induced 'despair' in the water maze, exploratory behavior and fear: effects of chronic antidepressant treatment. Neurobiol. Learn. Mem. 87, 624-634 (2007).
83. Schulz D, Huston JP, Buddenberg T, Topic B: 'Despair' induced by extinction trials in the water maze: relationship with measures of anxiety in aged and adult rats. Neurobiol. Learn. Mem. 87, 309-323. (2007).
84. De Leon MJ, Convit A, George AE et al.: In vivo structural studies of the hippocampus in normal aging and in Alzheimer's disease. Ann. NY Acad. Sci. 777, 1-13 (1996).
85. Jellinger K, Braak H, Braak E, Fischer P: Alzheimer lesions in the entorhinal region and isocortex in Parkinson's and Alzheimer's diseases. Ann. NY Acad Sci. 640, 203-209 (1991).
86. Farinelli M, Deschaux O, Hugues S, Thévenet A, Garcia R: Hippocampal train stimulation modulates recall of fear extinction independently of prefrontal cortex synaptic plasticity and lesions. Learn. Mem. 13, 329-334 (2006).
87. Hugues S, Garcia R: Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learn. Mem. 14, 520-524 (2007).
88. Maren S, Chang CH: Recent fear is resistant to extinction. Proc. Natl Acad. Sci. USA 103(47), 18020-18035 (2006).
89. Cahill L, Pham CA, Setlow B: Impaired memory consolidation in rats produced with β-adrenergic blockade. Neurobiol. Learn. Mem. 74, 259-266 (2000).
90. Henry M, Fishman JR. Youngner SJ: Propranolol and the prevention of post-traumatic stress disorder: is it wrong to crase the 'sting' of bad memories? Am. J. Bioeth. 7, 12-20 (2007).
91. Liao SM, Wasserman DT: Neuroethical concerns about mod rating traumatic memories. Am. J. Bioeth. 7(9), 38-40 (2007).
92. Izquierdo I: Memoria. ArtMed, Porto Alegre, Brazil (2002).