Can fear extinction be enhanced? A review of pharmacological and behavioral findings

Brain Research Bulletin

Volumn 105, Issue , 2014, Pages 46-60

  Fitzgerald, Paul J ^a   Seemann, Jocelyn R ^a   Maren, Stephen ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Context; Fluoxetine; L Dopa; Massed extinction; Propranolol; Yohimbine

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; ANANDAMIDE; ANTICONVULSIVE AGENT; BICUCULLINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABIDIOL; CITALOPRAM; CYCLOSERINE; CYTOCHROME C OXIDASE; DOPAMINE; ENDOCANNABINOID; FIBROBLAST GROWTH FACTOR 2; FLUOXETINE; METHYLENE BLUE; METHYLPHENIDATE; MUSCARINIC RECEPTOR BLOCKING AGENT; MUSCIMOL; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; NORADRENALIN; NORADRENALIN UPTAKE INHIBITOR; PICROTOXIN; PROPRANOLOL; QUINPIROLE; RIMONABANT; SCOPOLAMINE; SULPIRIDE; TANDOSPIRONE; UNINDEXED DRUG; YOHIMBINE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; LEVODOPA;

CALORIC RESTRICTION; CHOLINERGIC SYSTEM; CONDITIONING; FEAR; GENE EXPRESSION; HISTONE ACETYLATION; HUMAN; MEMORY CONSOLIDATION; NERVE EXCITABILITY; NONHUMAN; NORADRENALIN RELEASE; PRIORITY JOURNAL; REINFORCEMENT; REVIEW; SECOND MESSENGER; VIRTUAL REALITY EXPOSURE THERAPY; VISUAL STIMULATION; ANIMAL; CONDITIONED REFLEX; DRUG EFFECTS; PHYSIOLOGY;

ANIMALS; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; FLUOXETINE; HUMANS; LEVODOPA; NEUROTRANSMITTER AGENTS; PROPRANOLOL; YOHIMBINE;

EID: 84901505096     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2013.12.007     Document Type: Review

References (151)

1. Abraham A.D., Cunningham C.L., Lattal K.M. Methylphenidate enhances extinction of contextual fear. Learning and Memory 2012, 19:67-72.
2. Abumaria N., Yin B., Zhang L., Li X.Y., Chen T., Descalzi G., Zhao L., Ahn M., Luo L., Ran C., Zhuo M., Liu G. Effects of elevation of brain magnesium on fear conditioning, fear extinction, and synaptic plasticity in the infralimbic prefrontal cortex and lateral amygdala. Journal of Neuroscience 2011, 31:14871-14881.
3. Akirav I., Raizel H., Maroun M. Enhancement of conditioned fear extinction by infusion of the GABAA agonist muscimol into the rat prefrontal cortex and amygdala. European Journal of Neuroscience 2006, 23:758-764.
4. Andero R., Heldt S.A., Ye K., Liu X., Armario A., Ressler K.J. Effect of 7,8-dihydroxyflavone, a small-molecule TrkB agonist, on emotional learning. American Journal of Psychiatry 2011, 168:163-172.
5. Bahari-Javan S., Maddalena A., Kerimoglu C., Wittnam J., Held T., Bähr M., Burkhardt S., Delalle I., Kügler S., Fischer A., Sananbenesi F. HDAC1 regulates fear extinction in mice. Journal of Neuroscience 2012, 32:5062-5073.
6. Balooch S.B., Neumann D.L., Boschen M.J. Extinction treatment in multiple contexts attenuates ABC renewal in humans. Behaviour Research and Therapy 2012, 50:604-609.
7. Baum M., Andrus T., Jacobs W.J. Extinction of a conditioned emotional response: massed and distributed exposures. Behaviour Research and Therapy 1990, 28:63-68.
8. Berlau D., McGaugh J. Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiology of Learning and Memory 2006, 86:123-132.
9. Bitencourt R.M., Pamplona F.A., Takahashi R.N. Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. European Neuropsychopharmacology 2008, 18:849-859.
10. Blanchard R.J., Blanchard D.C. Crouching as an index of fear. Journal of Comparative and Physiological Psychology 1969, 67:370-375.
11. Bos M.G.N., Beckers T., Kindt M. The effects of noradrenergic blockade on extinction in humans. Biological Psychology 2012, 89:598-605.
12. Bouton M.E., Bolles R.C. Role of conditioned contextual stimuli in reinstatement of extinguished fear. Journal of Experimental Psychology: Animal Behavior Processes 1979, 5:368-378.
13. Bouton M.E., García-Gutiérrez A., Zilski J., Moody E.W. Extinction in multiple contexts does not necessarily make extinction less vulnerable to relapse. Behaviour Research and Therapy 2006, 44:983-994.
14. Bouton M.E., Kenney F.A., Rosengard C. State-dependent fear extinction with two benzodiazepine tranquilizers. Behavioral Neuroscience 1990, 104:44-55.
15. Bouton M.E., Mineka S., Barlow D.H. A modern learning theory perspective on the etiology of panic disorder. Psychological Review 2001, 108:4-32.
16. Bouton M.E., Vurbic D., Woods A.M. d-Cycloserine facilitates context-specific fear extinction learning. Neurobiology of Learning and Memory 2008, 90:504-510.
17. Bouton M.E., Westbrook R.F., Corcoran K.A., Maren S. Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biological Psychiatry 2006, 60:352-360.
18. Bowers M.E., Choi D.C., Ressler K.J. Neuropeptide regulation of fear and anxiety: implications of cholecystokinin, endogenous opioids, and neuropeptide Y. Physiology & Behavior 2012, 107:699-710.
19. Bredy T.W., Barad M. The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learning and Memory 2008, 15:39-45.
20. Bredy T.W., Wu H., Crego C., Zellhoefer J., Sun Y.E., Barad M. Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learning and Memory 2007, 14:268-276.
21. Brinks V., de Kloet E.R., Oitzl M.S. Corticosterone facilitates extinction of fear memory in BALB/c mice but strengthens cue related fear in C57BL/6 mice. Experimental Neurology 2009, 216:375-382.
22. Burghardt N.S., Sigurdsson T., Gorman J.M., McEwen B.S., LeDoux J.E. Chronic antidepressant treatment impairs the acquisition of fear extinction. Biological Psychiatry 2013, 73:1078-1086.
23. Cain C.K. Adrenergic transmission facilitates extinction of conditional fear in mice. Learning and Memory 2004, 11:179-187.
24. Cain C.K., Blouin A.M., Barad M. Temporally massed CS presentations generate more fear extinction than spaced presentations. Journal of Experimental Psychology 2003, 29:323-333.
25. Cammarota M., Barros D., Vianna M., Bevilaqua L., Coitinho A., Szapiro G., Izquierdo L., Median J., Izquierdo I. The transition from memory retrieval to extinction. Anais da Academia Brasileira de Ciencias 2004, 76:573-582.
26. Chan W.Y., Leung H.T., Westbrook R.F., McNally G.P. Effects of recent exposure to a conditioned stimulus on extinction of Pavlovian fear conditioning. Learning and Memory 2010, 17:512-521.
27. Chang C.-H., Maren S. Medial prefrontal cortex activation facilitates re-extinction of fear in rats. Learning and Memory 2011, 18:221-225.
28. Chang Y.-J., Yang C.-H., Liang Y.-C., Yeh C.-M., Huang C.-C., Hsu K.-S. Estrogen modulates sexually dimorphic contextual fear extinction in rats through estrogen receptor β. Hippocampus 2009, 19:1142-1150.
29. Chhatwal J.P., Davis M., Maguschak K.A., Ressler K.J. Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 2005, 30:516-524.
30. Choi D.C., Maguschak K.A., Ye K., Jang S.W., Myers K.M., Ressler K.J. Prelimbic cortical BDNF is required for memory of learned fear but not extinction or innate fear. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:2675-2680.
31. Craske M.G., Kircanski K., Zelikowsky M., Mystkowski J., Chowdhury N., Baker A. Optimizing inhibitory learning during exposure therapy. Behaviour Research and Therapy 2008, 46:5-27.
32. Das R.K., Kamboj S.K., Ramadas M., Yogan K., Gupta V., Redman E., Curran H.V., Morgan C.J.A. Cannabidiol enhances consolidation of explicit fear extinction in humans. Psychopharmacology 2013, 226:781-792.
33. Davis M., Walker D.L., Myers K.M. Role of the amygdala in fear extinction measured with potentiated startle. Annals of the New York Academy of Sciences 2003, 985:218-232.
34. de Quervain D., Bentz D., Michael T., Bolt O., Wiederhol B., Margraf J., Wilhelm F. Glucocorticoids enhance extinction-based psychotherapy. Proceedings of the National Academy of Science 2011, 108:6621-6625.
35. Deschaux O., Spennato G., Moreau J.-L., Garcia R. Chronic treatment with fluoxetine prevents the return of extinguished auditory-cued conditioned fear. Psychopharmacology 2011, 215:231-237.
36. Deschaux O., Zheng X., Lavigne J., Nachon O., Cleren C., Moreau J.-L., Garcia R. Post-extinction fluoxetine treatment prevents stress-induced reemergence of extinguished fear. Psychopharmacology 2012, 225:209-216.
37. Do-Monte F.H., Kincheski G.C., Pavesi E., Sordi R., Assreuy J., Carobrez A.P. Role of beta-adrenergic receptors in the ventromedial prefrontal cortex during contextual fear extinction in rats. Neurobiology of Learning and Memory 2010, 94:318-328.
38. Edelmann E., Lessmann V., Brigadski T. Pre- and postsynaptic twists in BDNF secretion and action in synaptic plasticity. Neuropharmacology 2013, [Epub ahead of print].
39. Estes W.K., Skinner B.F. Some quantitative properties of anxiety. Journal of Experimental Psychology 1941, 29:390-400.
40. Fanselow M.S. Conditioned and unconditional components of post-shock freezing. Pavlovian Journal of Biological Science 1980, 15:177-182.
41. Glautier S., Elgueta T., Nelson J.B. Extinction produces context inhibition and multiple-context extinction reduces response recovery in human predictive learning. Learning & Behavior 2013, [Epub ahead of print].
42. Gonzalez-Lima F., Bruchey A.K. Extinction memory improvement by the metabolic enhancer methylene blue. Learning and Memory 2004, 11:633-640.
43. Graham B.M., Langton J.M., Richardson R. Pharmacological enhancement of fear reduction: preclinical models. British Journal of Pharmacology 2011, 164:1230-1247.
44. Graham B.M., Richardson R. Acute systemic fibroblast growth factor-2 enhances long-term extinction of fear and reduces reinstatement in rats. Neuropsychopharmacology 2009, 34:1875-1882.
45. Graham B.M., Richardson R. Fibroblast growth factor-2 enhances extinction and reduces renewal of conditioned fear. Neuropsychopharmacology 2010, 35:1348-1355.
46. Graham B.M., Richardson R. Intraamygdala infusion of fibroblast growth factor 2 enhances extinction and reduces renewal and reinstatement in adult rats. Journal of Neuroscience 2011, 31:14151-14157.
47. Guastella A.J., Lovibond P.F., Dadds M.R., Mitchell P., Richardson R. A randomized controlled trial of the effect of d-cycloserine on extinction and fear conditioning in humans. Behaviour Research and Therapy 2007, 45:663-672.
48. Gunduz-Cinar O., MacPherson K.P., Cinar R., Gamble-George J., Sugden K., Williams B., Godlewski G., Ramikie T.S., Gorka A.X., Alapafuja S.O., Nikas S.P., Makriyannis A., Poulton R., Patel S., Hariri A.R., Caspi A., Moffitt T.E., Kunos G., Holmes A. Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity. Molecular Psychiatry 2012, 18:813-823.
49. Gunther L.M., Denniston J.C., Miller R.R. Conducting exposure treatment in multiple contexts can prevent relapse. Behaviour Research and Therapy 1998, 36:75-91.
50. Gutman A.R., Yang Y., Ressler K.J., Davis M. The role of neuropeptide Y in the expression and extinction of fear-potentiated startle. Journal of Neuroscience 2008, 28:12682-12690.
51. Haaker J., Gaburro S., Sah A., Gartmann N., Lonsdorf T., Meier K., Singewald N., Pape H., Morellini F., Kalisch R. Single dose of l-dopa makes extinction memories context-independent and prevents the return of fear. Proceedings of the National Academy of Science 2013, E2428-E2436.
52. Heinrichs S.C., Leite-Morris K.A., Rasmusson A.M., Kaplan G.B. Repeated valproate treatment facilitates fear extinction under specific stimulus conditions. Neuroscience Letters 2013, 552:108-113.
53. Holmes A., Quirk G.J. Pharmacological facilitation of fear extinction and the search for adjunct treatments for anxiety disorders - the case of yohimbine. Trends in Pharmacological Sciences 2010, 31:2-7.
54. Holmes N.M., Westbrook R.F. Extinction of reinstated or ABC renewed fear responses renders them resistant to subsequent ABA renewal. Journal of Experimental Psychology: Animal Behavior Processes 2013, 39:208-220.
55. Janak P.H., Corbit L.H. Deepened extinction following compound stimulus presentation: noradrenergic modulation. Learning and Memory 2010, 18:1-10.
56. Johnson J.S., Escobar M., Kimble W.L. Long-term maintenance of immediate or delayed extinction is determined by the extinction-test interval. Learning and Memory 2010, 17:639-644.
57. Jüngling K., Seidenbecher T., Sosulina L., Lesting J., Sangha S., Clark S.D., Okamura N., Duangdao D.M., Xu Y.-L., Reinscheid R.K., Pape H.-C. Neuropeptide S-mediated control of fear expression and extinction: role of intercalated GABAergic neurons in the amygdala. Neuron 2008, 59:298-310.
58. Kalish H.I. Strength of fear as a function of the number of acquisition and extinction trials. Journal of Experimental Psychology 1954, 47:1-9.
59. Kaplan G.B., Moore K.A. The use of cognitive enhancers in animal models of fear extinction. Pharmacology, Biochemistry and Behavior 2011, 99:217-228.
60. Karpova N.N., Pickenhagen A., Lindholm J., Tiraboschi E., Kulesskaya N., Agustsdottir A., Antila H., Popova D., Akamine Y., Sullivan R., Hen R., Drew L.J., Castren E. Fear erasure in mice requires synergy between antidepressant drugs and extinction training. Science 2011, 334:1731-1734.
61. Kindt M., Soeter M. Reconsolidation in a human fear conditioning study: a test of extinction as updating mechanism. Biological Psychology 2013, 92:43-50.
62. Klumpers F., Denys D., Kenemans J.L., Grillon C., van der Aart J., Baas J.M. Testing the effects of 9-THC and d-cycloserine on extinction of conditioned fear in humans. Journal of Psychopharmacology 2012, 26:471-478.
63. Knapska E., Maren S. Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learning and Memory 2009, 16:486-493.
64. Kuriyama K., Honma M., Soshi T., Fujii T., Kim Y. Effect of d-cycloserine and valproic acid on the extinction of reinstated fear-conditioned responses and habituation of fear conditioning in healthy humans: a randomized controlled trial. Psychopharmacology 2011, 218:589-597.
65. Laborda M.A., Miller R.R. Preventing return of fear in an animal model of anxiety: additive effects of massive extinction and extinction in multiple contexts. Behavior Therapy 2013, 44:249-261.
66. Lach G., de Lima T.C.M. Role of NPY Y1 receptor on acquisition, consolidation and extinction on contextual fear conditioning: dissociation between anxiety, locomotion and non-emotional memory behavior. Neurobiology of Learning and Memory 2013, 103:26-33.
67. Lafenêtre P., Chaouloff F., Marsicano G. The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacological Research 2007, 56:367-381.
68. Lattal K.M., Barrett R.M., Wood M.A. Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behavioral Neuroscience 2007, 121:1125-1131.
69. Ledgerwood L., Richardson R., Cranney J. d-Cycloserine facilitates extinction of learned fear: effects on reacquisition and generalized extinction. Biological Psychiatry 2005, 57:841-847.
70. LeDoux J.E., Sakaguchi A., Reis D.J. Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. Journal of Neuroscience 1984, 4:683-698.
71. Li A.-J., Suzuki S., Suzuki M., Mizukoshi E., Imamura T. Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons. European Journal of Neuroscience 2002, 16:1313-1324.
72. Li S.H., Westbrook R.F. Massed extinction trials produce better short-term but worse long-term loss of context conditioned fear responses than spaced trials. Journal of Experimental Psychology 2008, 34:336-351.
73. Lin H.-C., Mao S.-C., Su C.-L., Gean P.-W. The role of prefrontal cortex CB1 receptors in the modulation of fear memory. Cerebral Cortex 2009, 19:165-175.
74. Lovibond P.F., Davis N.R., O'Flahery A.S. Protection from extinction in human fear conditioning. Behaviour Research and Therapy 2000, 38:967-983.
75. MacKillop J., Lisman S.A. Effects of a context shift and multiple context extinction on reactivity to alcohol cues. Experimental and Clinical Psychopharmacology 2008, 16:322-331.
76. Malvaez M., McQuown S.C., Rogge G.A., Astarabadi M., Jacques V., Carreiro S., Rusche J.R., Wood M.A. HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:2647-2652.
77. Mao S.C. Extinction training in conjunction with a partial agonist of the glycine site on the NMDA receptor erases memory trace. Journal of Neuroscience 2006, 26:8892-8899.
78. Maren S. Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 2011, 70:830-845.
79. Maren S., Chang C. Recent fear is resistant to extinction. Proceedings of the National Academy of Science 2006, 103:18020-18025.
80. Maren S., Phan K.L., Liberzon I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nature Reviews Neuroscience 2013, 14:417-428.
81. Maren S., Holt W. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behavioural Brain Research 2000, 110:97-108.
82. Maren S., Quirk G.J. Neuronal signaling of fear memory. Nature Reviews Neuroscience 2004, 5:844-852.
83. Marsicano G., Wotjak 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.
84. Matsuda S., Matsuzawa D., Nakazawa K., Sutoh C., Ohtsuka H., Ishii D., Tomizawa H., Iyo M., Shimizu E. d-Serine enhances extinction of auditory cued fear conditioning via ERK1/2 phosphorylation in mice. Progress in Neuropsychopharmacology & Biological Psychiatry 2010, 34:895-902.
85. Matsumoto Y., Morinobu S., Yamamoto S., Matsumoto T., Takei S., Fujita Y., Yamawaki S. Vorinostat ameliorates impaired fear extinction possibly via the hippocampal NMDA-CaMKII pathway in an animal model of posttraumatic stress disorder. Psychopharmacology (Berl) 2013, 229:51-62.
86. McConnell B.L., Miguez G., Miller R.R. Extinction with multiple excitors. Learning & Behavior 2012, 41:119-137.
87. Milad M.R., Igoe S.A., Lebron-Milad K., Novales J.E. Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience 2009, 164:887-895.
88. Milad M.R., Quirk G.J. Fear extinction as a model for translational neuroscience: ten years of progress. Annual Review of Psychology 2012, 63:129-151.
89. Monfils M.H., Cowansage K.K., Klann E., LeDoux J.E. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 2009, 324:951-955.
90. Moody E.W., Sunsay C., Bouton M.E. Priming and trial spacing in extinction: effects on extinction performance, spontaneous recovery, and reinstatement in appetitive conditioning. The Quarterly Journal of Experimental Psychology 2006, 59:809-829.
91. Morris M.J., Mahgoub M., Na E.S., Pranav H., Monteggia L.M. Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. Journal of Neuroscience 2013, 33:6401-6411.
92. Morris R.W., Bouton M.E. The effect of yohimbine on the extinction of conditioned fear: a role for context. Behavioral Neuroscience 2007, 121:501-514.
93. Mueller D., Cahill S.P. Noradrenergic modulation of extinction learning and exposure therapy. Behavioural Brain Research 2010, 208:1-11.
94. 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 2009, 204:599-606.
95. Mueller D., Porter J.T., Quirk G.J. Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. Journal of Neuroscience 2008, 28:369-375.
96. Murchison C., Zhang X., Zhang W., Ouyang M., Lee A., Thomas S. A distinct role for norepinephrine in memory retrieval. Cell 2004, 117:131-143.
97. Myers K.M., Davis M. Behavioral and neural analysis of extinction. Neuron 2002, 36:567-584.
98. Neumann D.L., Lipp O.V., Cory S.E. Conducting extinction in multiple contexts does not necessarily attenuate the renewal of shock expectancy in a fear-conditioning procedure with humans. Behaviour Research and Therapy 2007, 45:385-394.
99. Okamura N., Garau C., Duangdao D.M., Clark S.D., Jüngling K., Pape H.-C., Reinscheid R.K. Neuropeptide S enhances memory during the consolidation phase and interacts with noradrenergic systems in the brain. Neuropsychopharmacology 2010, 36:744-752.
100. Orinstein A.J., Urcelay G.P., Miller R.R. Expanding the intertrial interval during extinction: response cessation and recovery. Behavior Therapy 2010, 41:14-29.
101. Orr S.P., Milad M.R., Metzger L.J., Lasko N.B., Gilbertson M.W., Pitman R.K. Effects of beta blockade, PTSD diagnosis, and explicit threat on the extinction and retention of an aversively conditioned response. Biological Psychology 2006, 73:262-271.
102. Ouyang M., Thomas S. A requirement for memory retrieval during and after long-term extinction learning. Proceedings of the National Academy of Science 2005, 102:9347-9352.
103. Pamplona F.A., Bitencourt R.M., Takahashi R.N. Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats. Neurobiology of Learning and Memory 2008, 90:290-293.
104. Pamplona F.A., Prediger R.D.S., Pandolfo P., Takahashi R.N. The cannabinoid receptor agonist WIN 55,212-2 facilitates the extinction of contextual fear memory and spatial memory in rats. Psychopharmacology 2006, 188:641-649.
105. Parnas A.S., Weber M., Richardson R. Effects of multiple exposures to d-cycloserine on extinction of conditioned fear in rats. Neurobiology of Learning and Memory 2005, 83:224-231.
106. Parsons T.D., Rizzo A.A. Affective outcomes of virtual reality exposure therapy for anxiety and specific phobias: a meta-analysis. Journal of Behavior Therapy and Experimental Psychiatry 2008, 39:250-261.
107. Pavlov I.P. Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex 1927, Oxford University Press.
108. 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.
109. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48:175-187.
110. Pitman R.K., Milad M.R., Igoe S.A., Vangel M.G., Orr S.P., Tsareva A., Gamache K., Nader K. Systemic mifepristone blocks reconsolidation of cue-conditioned fear; propranolol prevents this effect. Behavioral Neuroscience 2011, 125:632-638.
111. Ponnusamy R., Nissim H.A., Barad M. Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice. Learning and Memory 2005, 12:399-406.
112. Powers M.B., Smits J.A.J., Otto M.W., Sanders C., Emmelkamp P.M.G. Facilitation of fear extinction in phobic participants with a novel cognitive enhancer: a randomized placebo controlled trial of yohimbine augmentation. Journal of Anxiety Disorders 2009, 23:350-356.
113. Quirk G.J., Garcia R., González-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry 2006, 60:337-343.
114. Rabinak C.A., Angstadt M., Sripada C.S., Abelson J.L., Liberzon I., Milad M.R., Phan K.L. Cannabinoid facilitation of fear extinction memory recall in humans. Neuropharmacology 2013, 64:396-402.
115. Ren J., Li X., Zhang X., Li M., Wang Y., Ma Y. The effects of intra-hippocampal microinfusion of d-cycloserine on fear extinction, and the expression of NMDA receptor subunit NR2B and neurogenesis in the hippocampus in rats. Progress in Neuropsychopharmacology & Biological Psychiatry 2013, 44:257-264.
116. Rescorla R.A. Extinction can be enhanced by a concurrent excitor. Journal of Experimental Psychology: Animal Behavior Processes 2000, 26:251-260.
117. Ressler K., Rothbaum B., Tannenbaum L., Anderson P., Graao K., Zimand E., Hodges L., Davis M. Cognitive enhancers as adjuncts to psychotherapy. Archives of General Psychiatry 2004, 61:1136-1144.
118. Riddle M.C., McKenna M.C., Yoon Y.J., Pattwell S.S., Santos P.M.G., Casey B.J., Glatt C.E. Caloric restriction enhances fear extinction learning in mice. Neuropsychopharmacology 2013, 38:930-937.
119. Rodrigues S.M., LeDoux J.E., Sapolsky R.M. The influence of stress hormones on fear circuitry. Annual Review of Neuroscience 2009, 32:289-313.
120. Rodriguez-Romaguera J., Sotres-Bayon F., Mueller D., Quirk G.J. Systemic propranolol acts centrally to reduce conditioned fear in rats without impairing extinction. Biological Psychiatry 2009, 65:887-892.
121. Roozendaal B., McGaugh J.L. Memory modulation. Behavioral Neuroscience 2011, 125:797-824.
122. Rothbaum B.O., Hodges L.F. The use of virtual reality exposure in the treatment of anxiety disorders. Behavior Modification 1999, 23:507-525.
123. Ruehle S., Remmers F., Romo-Parra H., Massa F., Wickert M., Wortge S., Haring M., Kaiser N., Marsicano G., Pape H.C., Lutz B. Cannabinoid CB1 receptor in dorsal telencephalic glutamatergic neurons: distinctive sufficiency for hippocampus-dependent and amygdala-dependent synaptic and behavioral functions. Journal of Neuroscience 2013, 33:10264-10277.
124. Saito Y., Matsumoto M., Yanagawa Y., Hiraide S., Inoue S., Kubo Y., Shimamura K.-I., Togashi H. Facilitation of fear extinction by the 5-HT1A receptor agonist tandospirone: possible involvement of dopaminergic modulation. Synapse 2012, 67:161-170.
125. Santini E., Porter J.T. M-type potassium channels modulate the intrinsic excitability of infralimbic neurons and regulate fear expression and extinction. Journal of Neuroscience 2010, 30:12379-12386.
126. Schiller D., Kanen J.W., Ledoux J.E., Monfils M.H., Phelps E.A. Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement. Proceedings of the National Academy of Sciences of the United States of America 2013, [Epub ahead of print].
127. 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.
128. Shiban Y., Pauli P., Muhlberger A. Effect of multiple context exposure on renewal in spider phobia. Behaviour Research and Therapy 2013, 51:68-74.
129. Shipley R.H. Extinction of conditioned fear in rats as a function of several parameters of CS exposure. Journal of Comparative and Physiological Psychology 1974, 87:699-707.
130. Si W., Aluisio L., Okamura N., Clark S.D., Fraser I., Sutton S.W., Bonaventure P., Reinscheid R.K. Neuropeptide S stimulates dopaminergic neurotransmission in the medial prefrontal cortex. Journal of Neurochemistry 2010, 115:475-482.
131. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable roles of prelimbic and infralimbic cortices ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 2010, 36:529-538.
132. Smits J.A.J., Rosenfield D., Otto M.W., Powers M.B., Hofmann S.G., Telch M.J., Pollack M.H., Tart C.D. d-Cycloserine enhancement of fear extinction is specific to successful exposure sessions: evidence from the treatment of height phobia. Biological Psychiatry 2013, 73:1054-1058.
133. Soeter M., Kindt M. Disrupting reconsolidation: pharmacological and behavioral manipulations. Learning and Memory 2011, 18:357-366.
134. Soeter M., Kindt M. Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology 2011, 37:1204-1215.
135. Spennato G., Zerbib C., Mondadori C., Garcia R. Fluoxetine protects hippocampal plasticity during conditioned fear stress and prevents fear learning potentiation. Psychopharmacology 2008, 196:583-589.
136. Toth I., Dietz M., Peterlik D., Huber S.E., Fendt M., Neumann I.D., Flor P.J., Slattery D.A. Pharmacological interference with metabotropic glutamate receptor subtype 7 but not subtype 5 differentially affects within- and between-session extinction of Pavlovian conditioned fear. Neuropharmacology 2012, 62:1619-1626.
137. Urcelay G.P., Lipatova O., Miller R.R. Constraints on enhanced extinction resulting from extinction treatment in the presence of an added excitor. Learning and Motivation 2009, 40:343-363.
138. Urcelay G.P., Wheeler D.S., Miller R.R. Spacing extinction trials alleviates renewal and spontaneous recovery. Learning & Behavior 2009, 37:60-73.
139. Vansteenwegen D., Vervliet B., Iberico C., Baeyens F., Van den Bergh O., Hermans D. The repeated confrontation with videotapes of spiders in multiple contexts attenuates renewal of fear in spider-anxious students. Behaviour Research and Therapy 2007, 45:1169-1179.
140. Verma D., Tasan R.O., Herzog H., Sperk G. NPY controls fear conditioning and fear extinction by combined action on Y1 and Y2 receptors. British Journal of Pharmacology 2012, 166:1461-1473.
141. Vervliet B., Vansteenwegen D., Hermans D., Eelen P. Concurrent excitors limit the extinction of conditioned fear in humans. Behaviour Research and Therapy 2007, 45:375-383.
142. Walker D., Ressler K., Lu K., Davis M. Facilitation of conditioned fear extinction by systemic administration or intra-amygdalar infusions of d-cycloserine as assessed with fear-potentiated startle in rats. The Journal of Neuroscience 2002, 22:2343-2351.
143. Weber M., Hart J., Richardson R. Effects of d-cycloserine on extinction of learned fear to an olfactory cue. Neurobiology of Learning and Memory 2007, 87:476-482.
144. Wei W., Coelho C., Li X., Marek R., Yan S., Anderson S., Meyers D., Mukherjee C., Sbardella G., Castellano S., Milite C., Rotili D., Mai A., Cole P., Sah P., Kobor M., Bredy T. p300/CBP-associated factor selectively regulates the extinction of conditioned fear. The Journal of Neuroscience 2012, 32:11930-11941.
145. Woods A.M., Bouton M.E. d-Cycloserine facilitates extinction but does not eliminate renewal of the conditioned emotional response. Behavioral Neuroscience 2006, 120:1159-1162.
146. Yang Y.-L., Chao P.-K., Lu K.-T. Systemic and intra-amygdala administration of glucocorticoid agonist and antagonist modulate extinction of conditioned fear. Neuropsychopharmacology 2006, 31:912-924.
147. Yang Y.-L., Chao P.-K., Ro L.-S., Wo Y.-Y.P., Lu K.-T. Glutamate NMDA receptors within the amygdala participate in the modulatory effect of glucocorticoids on extinction of conditioned fear in rats. Neuropsychopharmacology 2007, 32:1042-1051.
148. Yang Y.L., Lu K.T. Facilitation of conditioned fear extinction by d-cycloserine is mediated by mitogen-activated protein kinase and phosphatidylinositol 3-kinase cascades and requires de novo protein synthesis in basolateral nucleus of amygdala. Neuroscience 2005, 134:247-260.
149. Zechel S., Werner S., Unsicker K., von Bohlen und Halbach O. Expression and functions of fibroblast growth factor 2 (FGF-2) in hippocampal formation. The Neuroscientist 2010, 16:357-373.
150. Zelikowsky M., Hast T.A., Bennett R.Z., Merjanian M., Nocera N.A., Ponnusamy R., Fanselow M.S. Cholinergic blockade frees fear extinction from its contextual dependency. Biological Psychiatry 2013, 73:345-352.
151. Zushida K., Sakurai M., Wada K., Sekiguchi M. Facilitation of extinction learning for contextual fear memory by PEPA: a potentiator of AMPA receptors. Journal of Neuroscience 2007, 27:158-166.