Deficits in conditioned fear extinction in obsessive-compulsive disorder and neurobiological changes in the fear circuit

JAMA Psychiatry

Volumn 70, Issue 6, 2013, Pages 608-618

  Milad, Mohammed R ^a   Furtak, Sharon C ^a,c   Greenberg, Jennifer L ^a   Keshaviah, Aparna ^a   Im, Jooyeon J ^a   Falkenstein, Martha J ^a   Jenike, Michael ^a   Rauch, Scott L ^b   Wilhelm, Sabine ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MCLEAN HOSPITAL   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BLOOD OXYGENATION; CASE CONTROL STUDY; CEREBELLUM; CLINICAL ARTICLE; CONDITIONING; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ELECTRODERMAL RESPONSE; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; MALE; NEUROBIOLOGY; OBSESSIVE COMPULSIVE DISORDER; POSTERIOR CINGULATE; PUTAMEN; RECALL; VENTROMEDIAL PREFRONTAL CORTEX;

EID: 84878646314     PISSN: 2168622X     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamapsychiatry.2013.914     Document Type: Article

References (61)

1. Milad MR, Rauch SL. Obsessive-compulsive disorder: beyond segregated corticostriatal pathways. Trends Cogn Sci. 2012;16(1):43-51.
2. Milad MR, Quirk GJ. Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol. 2012;63:129-151.
3. Pare D, Duvarci S. Amygdala microcircuits mediating fear expression and extinction. Curr Opin Neurobiol. 2012;22(4):717-723.
4. Graham BM, Milad MR. The study of fear extinction: implications for anxiety disorders. Am J Psychiatry. 2011;168(12):1255-1265.
5. Linnman C, Rougemont-Bücking A, Beucke JC, Zeffiro TA, Milad MR. Unconditioned responses and functional fear networks in human classical conditioning. Behav Brain Res. 2011;221(1):237-245.
6. Linnman C, Zeidan MA, Pitman RK, Milad MR. Reprint of: Resting cerebral metabolism correlates with skin conductance and functional brain activation during fear conditioning. Biol Psychol. 2013;92(1):26-35.
7. Klucken T, Schweckendiek J, Koppe G, et al. Neural correlates of disgust- and fear-conditioned responses. Neuroscience. 2012;201:209-218.
8. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron. 1998;20(5):937-945. (Pubitemid 28247399)
9. Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL. A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry. 2007;62(10):1191-1194. (Pubitemid 350029727)
10. 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 Psychiatry. 2007;62(5):446-454. (Pubitemid 47284021)
11. Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron. 2004;43(6):897-905. (Pubitemid 39215019)
12. Kalisch R, Korenfeld E, Stephan KE, Weiskopf N, Seymour B, Dolan RJ. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J Neurosci. 2006;26(37):9503-9511. (Pubitemid 44396863)
13. Holt DJ, Lebron-Milad K, Milad MR, et al. Extinction memory is impaired in schizophrenia. Biol Psychiatry. 2009;65(6):455-463.
14. Milad MR, Pitman RK, Ellis CB, et al. Neurobiological basis for failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry. 2009;66(12):1075-1082.
15. Rougemont-Bücking A, Linnman C, Zeffiro TA, et al. Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neurosci Ther. 2011;17(4):227-236.
16. Jovanovic T, Norrholm SD, Blanding NQ, et al. Impaired fear inhibition is a biomarker of PTSD but not depression. Depress Anxiety. 2010;27(3):244-251.
17. Blechert J, Michael T, Vriends N, Margraf J, Wilhelm FH. Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behav Res Ther. 2007;45(9):2019-2033. (Pubitemid 47210952)
18. Michael T, Blechert J, Vriends N, Margraf J, Wilhelm FH. Fear conditioning in panic disorder: enhanced resistance to extinction. J Abnorm Psychol. 2007;116(3):612-617. (Pubitemid 47444697)
19. Orr SP, Metzger LJ, Lasko NB, Macklin ML, Peri T, Pitman RK. De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder. J Abnorm Psychol. 2000;109(2):290-298. (Pubitemid 30616926)
20. Wilhelm S, Tolin DF, Steketee G. Challenges in treating obsessive-compulsive disorder: introduction. J Clin Psychol. 2004;60(11):1127-1132. (Pubitemid 39392085)
21. Yücel M, Harrison BJ, Wood SJ, et al. Functional and biochemical alterations of the medial frontal cortex in obsessive-compulsive disorder. Arch Gen Psychiatry. 2007;64(8):946-955. (Pubitemid 47230618)
22. Cardoner N, Harrison BJ, Pujol J, et al. Enhanced brain responsiveness during active emotional face processing in obsessive compulsive disorder. World J Biol Psychiatry. 2011;12(5):349-363.
23. Mataix-Cols D, Wooderson S, Lawrence N, Brammer MJ, Speckens A, Phillips ML. Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Arch Gen Psychiatry. 2004;61(6):564-576. (Pubitemid 38747311)
24. Dougherty DD, Baer L, Cosgrove GR, et al. Prospective long-term follow-up of 44 patients who received cingulotomy for treatment-refractory obsessive-compulsive disorder. Am J Psychiatry. 2002;159(2):269-275. (Pubitemid 34126905)
25. Perani D, Colombo C, Bressi S, et al. [18F]FDG PET study in obsessive-compulsive disorder. A clinical/metabolic correlation study after treatment. Br J Psychiatry. 1995;166(2):244-250.
26. Rauch SL, Milad MR, Orr SP, Quinn BT, Fischl B, Pitman RK. Orbitofrontal thickness, retention of fear extinction, and extraversion. Neuroreport. 2005;16(17):1909-1912. (Pubitemid 41653512)
27. Milad MR, Rauch SL. The role of the orbitofrontal cortex in anxiety disorders. Ann N Y Acad Sci. 2007;1121:546-561.
28. Linnman C, Zeidan MA, Furtak SC, Pitman RK, Quirk GJ, Milad MR. Resting amygdala and medial prefrontal metabolism predicts functional activation of the fear extinction circuit. Am J Psychiatry. 2012;169(4):415-423.
29. Goodman WK, Price LH, Rasmussen SA, et al. The Yale-Brown Obsessive Compulsive Scale, II: validity. Arch Gen Psychiatry. 1989;46(11):1012-1016. (Pubitemid 19278230)
30. Goodman WK, Price LH, Rasmussen SA, et al. The Yale-Brown Obsessive Compulsive Scale, I: development, use, and reliability. Arch Gen Psychiatry. 1989;46(11):1006-1011. (Pubitemid 19278229)
31. Zeidan MA, Igoe SA, Linnman C, et al. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol Psychiatry. 2011;70(10):920-927.
32. Linnman C, Zeidan MA, Pitman RK, Milad MR. Resting cerebral metabolism correlates with skin conductance and functional brain activation during fear conditioning. Biol Psychol. 2012;89(2):450-459.
33. Del Casale A, Kotzalidis GD, Rapinesi C, et al. Functional neuroimaging in obsessive-compulsive disorder. Neuropsychobiology. 2011;64(2):61-85.
34. Bremner JD, Vermetten E, Schmahl C, et al. Positron emission tomographic imaging of neural correlates of a fear acquisition and extinction paradigm in women with childhood sexual-abuse-related post-traumatic stress disorder. Psychol Med. 2005;35(6):791-806. (Pubitemid 40873380)
35. Klucken T, Kagerer S, Schweckendiek J, Tabbert K, Vaitl D, Stark R. Neural, electrodermal and behavioral response patterns in contingency aware and unaware subjects during a picture-picture conditioning paradigm. Neuroscience. 2009;158(2):721-731.
36. Schiller D, Levy I, Niv Y, LeDoux JE, Phelps EA. From fear to safety and back: reversal of fear in the human brain. J Neurosci. 2008;28(45):11517-11525.
37. Ferreira TL, Moreira KM, Ikeda DC, Bueno OF, Oliveira MG. Effects of dorsal striatum lesions in tone fear conditioning and contextual fear conditioning. Brain Res. 2003;987(1):17-24. (Pubitemid 37267882)
38. Corcoran KA, Desmond TJ, Frey KA, Maren S. Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J Neurosci. 2005;25(39):8978-8987. (Pubitemid 41384466)
39. Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ. Induction of fear extinction with hippocampal-infralimbic BDNF. Science. 2010;328(5983):1288-1290.
40. Rauch SL, Wedig MM, Wright CI, et al. Functional magnetic resonance imaging study of regional brain activation during implicit sequence learning in obsessive-compulsive disorder. Biol Psychiatry. 2007;61(3):330-336. (Pubitemid 46108676)
41. Atmaca M, Yildirim H, Ozdemir H, et al. Hippocampus and amygdalar volumes in patients with refractory obsessive-compulsive disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32(5):1283-1286.
42. Büchel C, Morris J, Dolan RJ, Friston KJ. Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron. 1998;20(5):947-957. (Pubitemid 28247400)
43. Knight DC, Smith CN, Cheng DT, Stein EA, Helmstetter FJ. Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning. Cogn Affect Behav Neurosci. 2004;4(3):317-325. (Pubitemid 39350497)
44. Stern ER, Welsh RC, Fitzgerald KD, et al. Hyperactive error responses and altered connectivity in ventromedial and frontoinsular cortices in obsessive-compulsive disorder. Biol Psychiatry. 2011;69(6):583-591.
45. Milad MR, Pitman RK, Ellis CB, et al. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry. 2009;66(12):1075-1082.
46. Holt DJ, Coombs G, Zeidan MA, Goff DC, Milad MR. Failure of neural responses to safety cues in schizophrenia. Arch Gen Psychiatry. 2012;69(9):893-903.
47. Fitzgerald KD, Stern ER, Angstadt M, et al. Altered function and connectivity of the medial frontal cortex in pediatric obsessive-compulsive disorder. Biol Psychiatry. 2010;68(11):1039-1047.
48. Fitzgerald KD, Welsh RC, Gehring WJ, et al. Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder. Biol Psychiatry. 2005;57(3):287-294. (Pubitemid 40187373)
49. Baxter LR Jr, Saxena S, Brody AL, et al. Brain mediation of obsessive-compulsive disorder symptoms: evidence from functional brain imaging studies in the human and nonhuman primate. Semin Clin Neuropsychiatry. 1996;1(1):32-47.
50. Menzies L, Chamberlain SR, Laird AR, Thelen SM, Sahakian BJ, Bullmore ET. Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav Rev. 2008;32(3):525-549. (Pubitemid 351173336)
51. Sacchetti B, Sacco T, Strata P. Reversible inactivation of amygdala and cerebellum but not perirhinal cortex impairs reactivated fear memories. Eur J Neurosci. 2007;25(9):2875-2884. (Pubitemid 46888826)
52. Robleto K, Thompson RF. Extinction of a classically conditioned response: red nucleus and interpositus. J Neurosci. 2008;28(10):2651-2658. (Pubitemid 351348206)
53. Nabeyama M, Nakagawa A, Yoshiura T, et al. Functional MRI study of brain activation alterations in patients with obsessive-compulsive disorder after symptom improvement. Psychiatry Res. 2008;163(3):236-247.
54. Page LA, Rubia K, Deeley Q, et al. A functional magnetic resonance imaging study of inhibitory control in obsessive-compulsive disorder. Psychiatry Res. 2009;174(3):202-209.
55. Tobe RH, Bansal R, Xu D, et al. Cerebellar morphology in Tourette syndrome and obsessive-compulsive disorder. Ann Neurol. 2010;67(4):479-487.
56. Craig AD. How do you feel - now? the anterior insula and human awareness. Nat Rev Neurosci. 2009;10(1):59-70.
57. Olatunji BO. Changes in disgust correspond with changes in symptoms of contamination-based OCD: a prospective examination of specificity. J Anxiety Disord. 2010;24(3):313-317.
58. Storch EA, Murphy TK, Goodman WK, et al. A preliminary study of D-cycloserine augmentation of cognitive-behavioral therapy in pediatric obsessive-compulsive disorder. Biol Psychiatry. 2010;68(11):1073-1076.
59. Wilhelm S, Buhlmann U, Tolin DF, et al. Augmentation of behavior therapy with D-cycloserine for obsessive-compulsive disorder. Am J Psychiatry. 2008;165(3):335-341, quiz 409.
60. Storch EA, Merlo LJ, Bengtson M, et al. D-cycloserine does not enhance exposure-response prevention therapy in obsessive-compulsive disorder. Int Clin Psychopharmacol. 2007;22(4):230-237. (Pubitemid 46801947)
61. Davis M, Myers KM, Chhatwal J, Ressler KJ. Pharmacological treatments that facilitate extinction of fear: relevance to psychotherapy. NeuroRx. 2006;3(1):82-96. (Pubitemid 43276635)