Opposing effects of d-cycloserine on fear despite a common extinction duration: Interactions between brain regions and behavior

Neurobiology of Learning and Memory

Volumn 113, Issue , 2014, Pages 25-34

  Bolkan, Scott S ^a   Lattal, K Matthew ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Amygdala; Consolidation; D Cycloserine; Extinction; Fear; Hippocampus; Reconsolidation

Indexed keywords

CYCLOSERINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TUBERCULOSTATIC AGENT;

ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN REGION; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; FEAR; FREEZING; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; REINFORCEMENT; AGONISTS; ANIMAL; C57BL MOUSE; CATALEPSY; CONDITIONED REFLEX; DRUG EFFECTS; PHYSIOLOGY; TIME;

AMYGDALA; ANIMALS; ANTIBIOTICS, ANTITUBERCULAR; CONDITIONING, CLASSICAL; CYCLOSERINE; EXTINCTION, PSYCHOLOGICAL; FEAR; FREEZING REACTION, CATALEPTIC; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, N-METHYL-D-ASPARTATE; TIME FACTORS;

EID: 84902115442     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.12.009     Document Type: Article

References (77)

1. A agonist in the amygdala. Neuropsychopharmacology 2007, 32(3):542-550.
2. Akirav I., Segev A., Motanis H., Maroun M. d-Cycloserine into the BLA reverses the impairing effects of exposure to stress on the extinction of contextual fear, but not conditioned taste aversion. Learning and Memory 2009, 16(11):682-686.
3. Baker K.D., McNally G.P., Richardson R. d-Cycloserine does not facilitate fear extinction by reducing conditioned stimulus processing or promoting conditioned inhibition to contextual cues. Learning and Memory 2012, 19(10):461-469.
4. Bouton M.E. Context, ambiguity, and unlearning: Sources of relapse after behavioral extinction. Biological Psychiatry 2002, 52:976-986.
5. Bouton M.E., Vurbic D., Woods A.M. d-Cycloserine facilitates context-specific fear extinction learning. Neurobiology of Learning and Memory 2008, 90(3):504-510.
6. Bush D.E., Sotres-Bayon F., LeDoux J.E. Individual differences in fear: Isolating fear reactivity and fear recovery phenotypes. Journal of Traumatic Stress 2007, 20:413-422.
7. Busti D., Geracitano R., Whittle N., Dalezios Y., Manko M., Kaufmann W., et al. Different fear states engage distinct networks within the intercalated cell clusters of the amygdala. Journal of Neuroscience 2011, 31:5131-5144.
8. Chang C., Maren S. Medial prefrontal cortex activation facilitates re-extinction of fear in rats. Learning and Memory 2011, 18:221-225.
9. Cole S., McNally G.P. Temporal-difference prediction errors and Pavlovian fear conditioning: Role of NMDA and opioid receptors. Behavioral Neuroscience 2007, 121:1043-1052.
10. Cole S., McNally G.P. Complementary roles for amygdala and periaqueductal gray in temporal-difference fear learning. Learning and Memory 2009, 16:1-7.
11. Corcoran K.A., Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. Journal of Neuroscience 2001, 21:1720-1726.
12. Davis M. NMDA receptors and fear extinction: Implications for cognitive behavioral therapy. Dialogues in Clinical Neuroscience 2011, 13(4):463-474.
13. de Kleine R.A., Hendriks G.J., Kusters W.J., Broekman T.G., van Minnen A. A randomized placebo-controlled trial of d-cycloserine to enhance exposure therapy for posttraumatic stress disorder. Biological Psychiatry 2012, 2012(71):962-968.
14. Difede J., Cukor J., Wyka K., Olden M., Hoffman H., Lee F.S., et al. d-Cycloserine augmentation of exposure therapy for posttraumatic stress disorder: A pilot randomized clinical trial. Neuropsychopharmacology 2013, 10.1038/npp.2013.317.
15. Ehrlich I., Humeau Y., Grenier F., Ciocchi S., Herry C., Luthi A. Amygdala inhibitory circuits and the control of fear memory. Neuron 2009, 62:757-771.
16. Fanselow M.S. Learning theory and neuropsychology: Configuring their disparate elements in the hippocampus. Journal of Experimental Psychology: Animal Behavior Processes 1999, 25:275-283.
17. Flavell C.R., Barber D.J., Lee J.L. Behavioural memory reconsolidation of food and fear memories. Nature Communications 2011, 2:504.
18. Ganasen K.A., Ipser J.C., Stein D.J. Augmentation of cognitive behavioral therapy with pharmacotherapy. Psychiatric Clinics of North America 2010, 33(3):687-699.
19. Griebel G., Holmes A. 50 years of hurdles and hope in anxiolytic drug discovery. Nature Reviews Drug Discovery 2013, 12:1-21.
20. Groblewski P.A., Lattal K.M., Cunningham C.L. Effects of d-Cycloserine on extinction and reconditioning of ethanol-seeking behavior in mice. Alcoholism, Clinical and Experimental Research 2009, 33(5):772-782.
21. Guastella A.J., Dadds M.R., Lovibond P.F., Mitchell P., Richardson G.A. A randomized controlled trial of the effect of d-cycloserine on exposure therapy for spider fear. Journal of Psychiatric Research 2007, 41:466-471.
22. 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(4):663-672.
23. Guastella A.J., Richardson R., Lovibond P.F., Rapee R.M., Gaston J.E., Mitchell P., et al. A randomized controlled trial of d-cylcoserine enhancement of exposure therapy for social anxiety disorder. Biological Psychiatry 2008, 63:544-549.
24. Hefner K., Whittle N., Juhasz J., Norcross M., Karlsson R.M., Saksida L.M., et al. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. Journal of Neuroscience 2008, 28:8074-8085.
25. Herry C., Ciocchi S., Senn V., Demmou L., Muller C., Luthi A. Switching on and off fear by distinct neuronal circuits. Nature 2008, 454(7204):600-606.
26. Hofmann S.G. Cognitive processes during fear acquisition and extinction in animals and humans: Implications for exposure therapy of anxiety disorders. Clinical Psychology Review 2008, 28(2):199-210.
27. Hofmann S.G., Meuret A.E., Smits J.A., Simon N.M., Pollack M.H., Eisenmenger K., et al. Augmentation of exposure therapy for social anxiety disorder with d-cycloserine. Archives of General Psychiatry 2006, 63:298-304.
28. Hofmann S.G., Smits J.A.J., Asnaani A., Gutner C.A., Otto M.W. Cognitive enhancers for anxiety disorders. Pharmacology Biochemistry and Behavior 2011, 99:275-284.
29. Holmes A., Singewald N. Individual differences in recovery from traumatic fear. Trends in Neuroscience 2013, 36(1):23-31.
30. Iordanova M.D. Dopamine transmission in the amygdala modulates surprise in an aversive blocking paradigm. Behavioral Neuroscience 2010, 124:780-788.
31. Langton J.M., Richardson R. d-Cycloserine facilitates extinction the first time but not the second time: An examination of the role of NMDA across the course of repeated extinction sessions. Neuropsychopharmacology 2008, 33:3096-3102.
32. Langton J.M., Richardson R. The effect of d-cycloserine on immediate vs. delayed extinction of learned fear. Learning and Memory 2010, 17:547-551.
33. Langton J.M., Richardson R. The temporal specificity of the switch from NMDAr-dependent extinction to NMDAr-independent re-extinction. Behavioural Brain Research 2010, 208:646-649.
34. Lattal K.M., Stafford J.M. What does it take to demonstrate memory erasure? Theoretical comment on Norrholm et al. (2008). Behavioral Neuroscience 2008, 122:1186-1190.
35. Lattal K.M., Wood M.A. Epigenetics and persistent memory: Implications for reconsolidation and silent extinction beyond zero. Nature Neuroscience 2013, 16(2):124-129.
36. Ledgerwood L., Richardson R., Cranney J. Effects of d-cycloserine on extinction of conditioned freezing. Behavioral Neuroscience 2003, 117:341-349.
37. Ledgerwood L., Richardson R., Cranney J. d-Cycloserine and the facilitation of extinction of conditioned fear: Consequences for reinstatement. Behavioral Neuroscience 2004, 118:505-513.
38. 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.
39. Lee J.L., Gardner R.J., Butler V.J., Everitt B.J. d-Cycloserine potentiates the reconsolidation of cocaine-associated memories. Learning and Memory 2009, 16:82-85.
40. Lee J.L., Milton A.L., Everitt B.J. Reconsolidation and extinction of conditioned fear: Inhibition and potentiation. Journal of Neuroscience 2006, 26:10051-10056.
41. Lehner M., Wislowska-Stanek A., Taracha E., Maciejak P., Szyndler J., Skorzewska A., et al. The effects of midazolam and d-cycloserine on the release of glutamate and GABA in the basolateral amygdala of low and high anxiety rats during extinction trial of a conditioned fear test. Neurobiology of Learning and Memory 2010, 94(4):468-480.
42. Leung H.T., Westbrook R.F. Spontaneous recovery of extinguished fear responses deepens their extinction: A role for error-correction mechanisms. Journal of Experimental Psychology: Animal Behavior Processes 2008, 34:461-474.
43. Likhtik E., Popa D., Apergis-Schoute J., Fidacaro G.A., Pare D. Amygdala intercalated neurons are required for expression of fear extinction. Nature 2008, 454(7204):642-645.
44. Likhtik E., Stujenske J.M., Topiwala M.A., Harris A.Z., Gordon J.A. Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nature Neuroscience 2013, 10.1038/nn.3582.
45. Litz B.T., Salters-Pedneault K., Steenkamp M.M., Hermos J.A., Bryant R.A., Otto M.W., et al. A randomized placebo-controlled trial of d-cycloserine and exposure therapy for posttraumatic stress disorder. Journal of Psychiatric Research 2012, 46:1184-1190.
46. MacPherson, et al. Temporal factors in the extinction of fear in inbred mouse strains differing in extinction efficacy. Biology of Mood & Anxiety Disorders 2013, 3(13).
47. Mao S.C., Hsiao Y.H., Gean P.W. Extinction training in conjunction with 865 a partial agonist of the glycine site on the NMDA receptor erases memory trace. Journal of Neuroscience 2006, 26(35):8892-8899.
48. Mao S.C., Lin H.C., Gean P.W. Augmentation of fear extinction by d-cycloserine is blocked by proteasome inhibitors. Neuropsychopharmacology 2008, 33(13):3085-3095.
49. Maren S. Synaptic mechanisms of associative memory in the amygdala. Neuron 2005, 7(6):783-786. (15).
50. McNally G.P., Johansen J.P., Blair H.T. Placing prediction into the fear circuit. Trends in neurosciences 2011, 34(6):283-292.
51. 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.
52. Milad M.R., Rauch S.L., Pitman R.K., Quirk G.J. Fear extinction in rats: Implications for human brain imaging and anxiety disorders. Biological Psychology 2006, 73:61-71.
53. Myers K., Davis M. Mechanisms of fear extinction. Molecular Psychiatry 2007, 12(2):120-150.
54. Nave A.M., Tolin D.F., Stevens M.C. Exposure therapy, d-cycloserine, and functional magnetic resonance imaging in patients with snake phobia: A randomized pilot study. Journal of Clinical Psychiatry 2012, 73(9):1179-1186.
55. Orsini C.A., Maren S. Neural and cellular mechanisms of fear and extinction memory formation. Neuroscience and Biobehavioral Reviews 2012, 36:1773-1802.
56. Pavlov, I. P. (1927). Conditioned reflexes, an investigation of the physiological activity of the cerebral cortex. London, Oxford University Press.
57. Portero-Tresserra M., Marti-Nicolovius M., Guillazo-Blanch G., Boadas-Vaello P., Vale-Martinez A. d-Cycloserine in the basolateral amygdala prevents extinction and enhances reconsolidation of odor-reward associative learning in rats. Neurobiology of Learning and Memory 2013, 100:1-11.
58. Przybyslawski J., Sara S.J. Reconsolidation of memory after its reactivation. Behavioural Brain Research 1997, 84:241-246.
59. Rachman S. The return of fear: Review and prospect. Clinical Psychology Review 1989, 9:147-168.
60. 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 Neuro-Psychopharmacology and Biological Psychiatry 2013, 44:257-264.
61. Rescorla R.A. Spontaneous recovery. Learning and Memory 2004, 11:501-509.
62. Rescorla R.A., Heth D. Reinstatement of fear to an extinguished conditioned stimulus. Journal of Experimental Psychology: Animal Behavior Processes 1975, 104:88-96.
63. Ressler K.J., Rothbaum B.O., Tannenbaum L., Anderson P., Graap K., Zimand E., et al. Cognitive enhancers as adjuncts to psychotherapy: Use of d-cycloserine in phobic individuals to facilitate extinction of fear. Archives of General Psychiatry 2004, 61:1136-1144.
64. Smits J.A., Rosenfield D., Otto M.W., Powers M.B., Hofmann S.G., Telch M.J., et al. 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.
65. Sotres-Bayon F., Corcoran K.A., Peters J., Sierra-Mercado D. Neural correlates of individual variability in fear extinction. Journal of Neuroscience 2008, 28:12147-12149.
66. Stafford J.M., Lattal K.M. Direct comparisons of the size and persistence of anisomycin-induced consolidation and reconsolidation deficits. Learning and Memory 2009, 16:494-503.
67. Stafford J.M., Maughan 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. Learning and Memory 2013, 20:156-163.
68. Stafford J.M., Raybuck J.D., Ryabinin A.E., Lattal K.M. Increasing histone-acetylation the hippocampus-infralimbic network enhances fear extinction. Biological Psychiatry 2012, 72(1):25-33.
69. Suzuki A., Josselyn S.A., Frankland P.W., Masushige S., Silva A.J., Kida S. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. Journal of Neuroscience 2004, 24:4787-4795.
70. Tart C.D., Handelsman P.R., Deboer L.B., Rosenfield D., Pollack M.H., Hofmann S.G., et al. Augmentation of exposure therapy with post-session administration of d-cycloserine. Journal of Psychiatric Research 2013, 47:168-174.
71. Vervliet B. Learning and memory in conditioned fear extinction: Effects of d-cycloserine. Acta Psychologica 2008, 127:601-613.
72. Walker D.L., Ressler K.J., Lu K.T., Davis M. Facilitation of conditioned fear extinction by systemic administration of intra-amygdala infusions of d-cycloserine as assessed with fear-poteniated startle in rats. Journal of Neuroscience 2002, 22:2343-2351.
73. 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.
74. Whittle N., Schmuckermair C., Gunduz Cinar O., Hauschild M., Ferraguti F., Holmes A., et al. Deep brain stimulation, histone deacetylase inhibitors and glutamatergic drugs rescue resistance to fear extinction in a genetic mouse model. Neuropharmacology 2013, 64:414-423.
75. 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.
76. Yamada D., Zushida K., Wada K., Sekiguchi M. Pharmacological discrimination of extinction and reconsolidation of contextual fear memory by a potentiator of AMPA receptors. Neuropsychopharmacology 2009, 34:2574-2584.
77. 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.