Predicting rapid response to cognitive-behavioural treatment for panic disorder: The role of hippocampus, insula, and dorsolateral prefrontal cortex

Behaviour Research and Therapy

Volumn 62, Issue , 2014, Pages 120-128

  Reinecke, Andrea ^a   Thilo, Kai ^b   Filippini, Nicola ^a,c   Croft, Alison ^d   Harmer, Catherine J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Oxford Psychologists Press   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d NONE   (United Kingdom)

Author keywords

Anxiety; CBT; Fear memory; Gray matter volume; Hippocampus; Insula; Prediction; Threat processing

Indexed keywords

ADULT; AGORAPHOBIA; AMYGDALOID NUCLEUS; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; BRAIN REGION; BRAIN SIZE; CLINICAL ARTICLE; COGNITION; COGNITIVE THERAPY; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; EMOTIONALITY; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HIPPOCAMPUS; HOSPITAL ANXIETY AND DEPRESSION SCALE; HUMAN; IMAGE ACQUISITION; IMAGE ANALYSIS; INSULA; LINGUAL GYRUS; MALE; MEMORY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL CORTEX; OUTCOME ASSESSMENT; PANIC; PANIC DISORDER SEVERITY SCALE; PREDICTION; PREFRONTAL CORTEX; PSYCHOMETRY; PUTAMEN; STRUCTURAL MAGNETIC RESONANCE IMAGING; SYMPTOMATOLOGY; THALAMUS; TRAINING; TREATMENT DURATION; TREATMENT RESPONSE; BRAIN CORTEX; MIDDLE AGED; NEUROIMAGING; ORGAN SIZE; PANIC DISORDER; PATHOLOGY; PATHOPHYSIOLOGY; PREDICTIVE VALUE; PROCEDURES; PROGNOSIS; TREATMENT OUTCOME;

ADULT; CEREBRAL CORTEX; COGNITIVE THERAPY; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROIMAGING; ORGAN SIZE; PANIC DISORDER; PREDICTIVE VALUE OF TESTS; PREFRONTAL CORTEX; PROGNOSIS; TREATMENT OUTCOME;

EID: 84910056294     PISSN: 00057967     EISSN: 1873622X     Source Type: Journal    
DOI: 10.1016/j.brat.2014.07.017     Document Type: Article

References (85)

1. Aaronson C.J., Shear M.K., Goetz R.R., Allen L.B., Barlow D.H., White K.S., et al. Predictors and time course of response among panic disorder patients treated with cognitive-behavioral therapy. Journal of Clinical Psychiatry 2008, 69(3):418-424.
2. Anagnostaras S.G., Gale G.D., Fanselow M.S. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 2001, 11(1):8-17.
3. Asthana M., Nueckel K., Muhlberger A., Neueder D., Polak T., Domschke K., et al. Effects of transcranial direct current stimulation on consolidation of fear memory. Frontiers in Psychiatry 2013, 4:107.
4. Ball T.M., Sullivan S., Flagan T., Hitchcock C.A., Simmons A., Paulus M.P., et al. Selective effects of social anxiety, anxiety sensitivity, and negative affectivity on the neural bases of emotional face processing. Neuroimage 2012, 59(2):1879-1887.
5. Ball T.M., Stein N.B., Ramsawh H.J., Campbell-Sills L., Paulus M.P. Single-subject anxiety treatment outcome prediction using functional neuroimaging. Neuropsychopharmacology 2014, 39:1254-1261.
6. Barbey A.K., Koenigs M., Grafman J. Dorsolateral prefrontal contributions to human working memory. Cortex 2013, 49(5):1195-1205.
7. Barlow D.H. Cognitive-behavioral therapy for panic disorder: Current status. Journal of ClinicalPsychiatry 1997, 58:32-37.
8. Barlow D.H., Gorman J.M., Shear M.K., Woods S.W. Cognitive-behavioral therapy, imipramine, or their combination for panic disorder: a randomized controlled trial. JAMA 2000, 283:2529-2536.
9. Beauregard M. Mind does really matter: evidence from neuroimaging studies of emotional self-regulation, psychotherapy, and placebo effect. Progress in Neurobiology 2007, 81(4):218-236.
10. Bouton M.E. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biological Psychiatry 2002, 52(10):976-986.
11. Chambless D.L., Caputo G.C., Bright P., Gallagher R. Assessment of fear of fear in agoraphobics - the body sensations questionnaire and the agoraphobic cognitions questionnaire. Journal of Consulting and Clinical Psychology 1984, 52(6):1090-1097.
12. Clark D.M., Salkovskis P.M., Ost L.G., Breitholtz E., Koehler K.A., Westling B.E., et al. Misinterpretation of body sensations in panic disorder. Journal of Consulting and Clinical Psychology 1997, 65(2):203-213.
13. Clum G.A., Clum G.A., Surls R. Ameta-analysis of treatments for panic disorder. Journal of Consulting and Clinical Psychology 1993, 61(2):317-326.
14. Craig A.D. How do you feel - now? The anterior insula and human awareness. Nature Reviews Neuroscience 2009, 10(1):59-70.
15. Craske M.G., Lang A.J., Tsao J.C.I., Mystkowski J.L., Rowe M.K. Reactivity to interoceptive cues in nocturnal panic. Journal of Behavior Therapy and Experimental Psychiatry 2001, 32(3):173-190.
16. Craske M.G., Street L., Barlow D.H. Instructions to focus upon or distract from internal cues during exposure treatment of agoraphobic avoidance. Behaviour Research and Therapy 1989, 27(6):663-672.
17. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nature Neuroscience 2004, 7(2):189-195.
18. Croft A., Hackmann A. Agoraphobia: an outreach treatment programme. Behavioural & Cognitive Psychotherapy 2013, 41:359-364.
19. De Cort K., Griez E., Buchler M., Schruers K. The role of "Interoceptive" fear conditioning in the development of panic disorder. Behavior Therapy 2012, 43(1):203-215.
20. Doehrmann O., Ghosh S.S., Polli F.E., Reynolds G.O., Horn F., Keshavan A., et al. Predicting treatment response in social anxiety disorder from functional magnetic resonance imaging. JAMA Psychiatry 2013, 70(1):87-97.
21. Dow M.G.T., Kenardy J.A., Johnston D.W., Newman M.G., Taylor C.B., Thomson A. Prognostic indices with brief and standard CBT for panic disorder: I. Predictors of outcome. Psychological Medicine 2007, 37(10):1493-1502.
22. Ehlers A., Breuer P., Dohn D., Fiegenbaum W. Heartbeat perception and panic disorder - possible explanations for discrepant findings. Behaviour Research and Therapy 1995, 33(1):69-76.
23. Etkin A. Functional neuroanatomy of anxiety: a neural circuit perspective. Behavioral neurobiology of anxiety and its treatment 2010, Vol. 2:251-277.
24. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 2007, 164(10):1476-1488.
25. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured clinical interview for DSM-IV axis I disorders, Clinician Version (SCID-CV) 1996, American Psychiatry Press, Inc, Washington, DC.
26. Foa E.B., Kozak M.J. Emotional processing of fear - exposure to corrective information. Psychological Bulletin 1986, 99(1):20-35.
27. Goldin P.R., Manber T., Hakimi S., Canli T., Gross J.J. Neural bases of social anxiety disorder emotional reactivity and cognitive regulation during social and physical threat. Archives of General Psychiatry 2009, 66(2):170-180.
28. Goossens L., Sunaert S., Peeters R., Griez E.J., Schruers K.R. Amygdala hyperfunction in phobic fear normalizes after exposure. Biological Psychiatry 2007, 62(10):1119-1125.
29. Gross J.J., John O.P. Individual differences in two emotion regulation processes: Implications for affect, relationships, and well-being. Journal of Personality and Social Psychology 2003, 85:348-362.
30. 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.
31. Hofmann S.G., Ellard K.K., Siegle G.J. Neurobiological correlates of cognitions in fear and anxiety: a cognitive-neurobiological information-processing model. Cognition & Emotion 2012, 26(2):282-299.
32. Hofmann S.G., Smits J.A., Rosenfield D., Simon N., Otto M.W., Meuret A.E., et al. D-Cycloserine as an augmentation strategy with cognitive-behavioral therapy for social anxiety disorder. American Journal of Psychiatry 2013, 170(7):751-758.
33. Holmes E.A., Craske M.G., Graybiel A.M. Psychological treatments: a call for mental-health science. Nature 2014, 511:287-289.
34. Houck P.R., Spiegel D.A., Shear M.K., Rucci P. Reliability of the self-report version of the panic disorder severity scale. Depression and Anxiety 2002, 15(4):183-185.
35. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17(2):825-841.
36. Kalisch R., Holt B., Petrovic P., De Martino B., Kloppel S., Buchel C., et al. The NMDA agonist D-cycloserine facilitates fear memory consolidation in humans. Cerebral Cortex 2009, 19(1):187-196.
37. Kamphuis J.H., Telch M.J. Effects of distraction and guided threat reappraisal on fear reduction during exposure-based treatments for specific fears. Behaviour Research and Therapy 2000, 38(12):1163-1181.
38. Kasper S., McEwen B.S. Neurobiological and clinical effects of the antidepressant tianeptine. CNS Drugs 2008, 22(1):15-26.
39. de Kleine R.A., Hendriks G.J., Kusters W.J., Broekman T.G., van Minnen A. Arandomized placebo-controlled trial of D-cycloserine to enhance exposure therapy for posttraumatic stress disorder. Biological Psychiatry 2012, 71(11):962-968.
40. Klumpp H., Fitzgerald D.A., Phan K.L. Neural predictors and mechanisms of cognitive behavioral therapy on threat processing in social anxiety disorder. Progress in Neuro-psychopharmacology & Biological Psychiatry 2013, 45:83-91.
41. Kushner M.G., Kim S.W., Donahue C., Thuras P., Adson D., Kotlyar M., et al. D-cycloserine augmented exposure therapy for obsessive-compulsive disorder. Biological Psychiatry 2007, 62(8):835-838.
42. Lang P.J., Bradley M.M., Cuthbert B.N. International affective picture system (IAPS): Technical manual and affective ratings 1997, National Institute of Mental Health Centre for the Study of Emotion and Attention, Gainesville, FL.
43. Lengersdorf D., Stuttgen M.C., Uengoer M., Gunturkun O. Transient inactivation of the pigeon hippocampus or the nidopallium caudolaterale during extinction learning impairs extinction retrieval in an appetitive conditioning paradigm. Behavioural Brain Research 2014, 265:93-100.
44. McClure E.B., Adler A., Monk C.S., Cameron J., Smith S., Nelson E.E., et al. fMRI predictors of treatment outcome in pediatric anxiety disorders. Psychopharmacology 2007, 191(1):97-105.
45. McGrath C.L., Kelley M.E., Holtzheimer P.E., Dunlop B.W., Craighead W.E., Franco A.R., et al. Toward a neuroimaging treatment selection biomarker for major depressive disorder. JAMA Psychiatry 2013, 70(8):821-829.
46. Mendlowicz M.V., Stein M.B. Quality of life in individuals with anxiety disorders. American Journal of Psychiatry 2000, 157(5):669-682.
47. Monfils M.-H., Cowansage K.K., Klann E., LeDoux J.E. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 2009, 324(5929):951-955.
48. Moro S.B., Cutini S., Ursini M.L., Ferrari M., Quaresima V. Prefrontal cortex activation during story encoding/retrieval: a multi-channel functional near-infrared spectroscopy study. Frontiers in Human Neuroscience 2013, 7.
49. Nelson H.E. National adult reading test (NART): Test manual 1982, NFER-Nelson, Windsor.
50. O'Rourke D., Fahy T.J., Brophy J., Prescott P. The galway study of panic disorder. III. Outcome at 5 to 6 years. British Journal of Psychiatry 1996, 168(4):462-469.
51. Ochsner K.N., Silvers J.A., Buhle J.T. Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Annals of the New York Academy of Sciences 2012, 1251:E1-E24.
52. Olatunji B.O., Ferreira-Garcia R., Caseras X., Fullana M.A., Wooderson S., Speckens A., et al. Predicting response to cognitive behavioral therapy in contamination-based obsessive-compulsive disorder from functional magnetic resonance imaging. Psychological Medicine 2013, 12:1-13.
53. Otto M.W., Pollack M.H., Maki K.M. Empirically supported treatments for panic disorder: costs, benefits, and stepped care. Journal of Consulting and Clinical Psychology 2000, 68(4):556-563.
54. Otto M.W., Tolin D.F., Simon N.M., Pearlson G.D., Basden S., Meunier S.A., et al. Efficacy of d-cycloserine for enhancing response to cognitive-behavior therapy for panic disorder. Biological Psychiatry 2010, 67(4):365-370.
55. Paquette V., Levesque J., Mensour B., Leroux J.M., Beaudoin G., Bourgouin P., et al. "Change the mind and you change the brain": effects of cognitive-behavioral therapy on the neural correlates of spider phobia. Neuroimage 2003, 18(2):401-409.
56. Patenaude B., Smith S.M., Kennedy D.N., Jenkinson M. ABayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 2011, 56(3):907-922.
57. Phan K.L., Fitzgerald D.A., Nathan P.J., Moore G.J., Uhde T.W., Tancer M.E. Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biological Psychiatry 2005, 57:210-219.
58. Pohlack S.T., Nees F., Liebscher C., Cacciaglia R., Diener S.J., Ridder S., et al. Hippocampal but not amygdalar volume affects contextual fear conditioning in humans. Human Brain Mapping 2012, 33(2):478-488.
59. Pollack M.H., Marzol P.C. Panic: course, complications and treatment of panic disorder. Journal of Psychopharmacology 2000, 14(2 Suppl.1):S25-S30.
60. Powers M.B., Smits J.A., Otto M.W., Sanders C., Emmelkamp P.M. 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(3):350-356.
61. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33(1):56-72.
62. Reinecke A., Harmer C. Acognitive-neuropsychological account of treatment action in anxiety: can we augment clinical efficacy?. Psychopathology Review 2014, (in press).
63. Reinecke A., Filippini N., Berna C., Western D.G., Hanson B., Cooper M.J., et al. Effective emotion regulation strategies improve fMRI and ECG markers of psychopathology in panic disorder: Implications for psychological treatment action 2014, (under review).
64. Reinecke A., Waldenmaier L., Cooper M.J., Harmer C.J. Changes in automatic threat processing precede and predict clinical changes with exposure-based cognitive-behavior therapy for panic disorder. Biological Psychiatry 2013, 73(11):1064-1070.
65. 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(11):1136-1144.
66. Rodriguez-Ortiz C.J., Balderas I., Saucedo-Alquicira F., Cruz-Castaneda P., Bermudez-Rattoni F. Long-term aversive taste memory requires insular and amygdala protein degradation. Neurobiology of Learning and Memory 2011, 95(3):311-315.
67. Roy-Byrne P., Sherbourne C., Miranda J., Stein M., Craske M., Golinelli D., et al. Poverty and response to treatment among panic disorder patients in primary care. American Journal of Psychiatry 2006, 163(8):1419-1425.
68. Sakamoto H., Fukuda R., Okuaki T., Rogers M., Kasai K., Machida T., et al. Parahippocampal activation evoked by masked traumatic images in posttraumatic stress disorder: a functional MRI study. Neuroimage 2005, 26(3):813-821.
69. Salkovskis P.M., Hackmann A., Wells A., Gelder M.G., Clark D.M. Belief disconfirmation versus habituation approaches to situational exposure in panic disorder with agoraphobia: a pilot study. Behaviour Research and Therapy 2007, 45(5):877-885.
70. Schienle A., Schafer A., Hermann A., Rohrmann S., Vaitl D. Symptom provocation and reduction in patients suffering from spider phobia: an fMRI study on exposure therapy. European Archives of Psychiatry and Clinical Neuroscience 2007, 257(8):486-493.
71. Shackman A.J., McMenamin B.W., Maxwell J.S., Greischar L.L., Davidson R.J. Right dorsolateral prefrontal cortical activity and behavioral inhibition. Psychological Science 2009, 20(12):1500-1506.
72. Sharp D.M., Power K.G., Simpson R.J., Swanson V., Moodie E., Anstee J.A., et al. Fluvoxamine, placebo, and cognitive behaviour therapy used alone and in combination in the treatment of panic disorder and agoraphobia. Journal of Anxiety Disorders 1996, 10(4):219-242.
73. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35(1):169-191.
74. Smith S.M. Fast robust automated brain extraction. Human Brain Mapping 2002, 17(3):143-155.
75. Smits J.A., Rosenfield D., Davis M.L., Julian K., Handelsman P.R., Otto M.W., et al. Yohimbine enhancement of exposure therapy for social anxiety disorder: a randomized controlled trial. Biological Psychiatry 2013, 16.
76. 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(4):804-812.
77. Stern E.R., Welsh R.C., Fitzgerald K.D., Gehring W.J., Lister J.J., Himle J.A., et al. Hyperactive error responses and altered connectivity in ventromedial and frontoinsular cortices in obsessive-compulsive disorder. Biological Psychiatry 2011, 69(6):583-591.
78. Straube T., Glauer M., Dilger S., Mentzel H.J., Miltner W.H. Effects of cognitive-behavioral therapy on brain activation in specific phobia. Neuroimage 2006, 29(1):125-135.
79. Taylor C.T., Alden L.E. Safety behaviors and judgmental biases in social anxiety disorder. Behaviour Research and Therapy 2010, 48(3):226-237.
80. Tsetsenis T., Ma X.-H., Lo Iacono L., Beck S.G., Gross C. Suppression of conditioning to ambiguous cues by pharmacogenetic inhibition of the dentate gyrus. Nature Neuroscience 2007, 10(7):896-902.
81. Vasa R.A., Pine D.S., Masten C.L., Vythilingam M., Collin C., Charney D.S., et al. Effects of yohimbine and hydrocortisone on panic symptoms, autonomic responses, and attention to threat in healthy adults. Psychopharmacology 2009, 204(3):445-455.
82. Weigand A., Grimm S., Astalosch A., Guo J.S., Briesemeister B.B., Lisanby S.H., et al. Lateralized effects of prefrontal repetitive transcranial magnetic stimulation on emotional working memory. Experimental Brain Research 2013, 227(1):43-52.
83. Woolrich M.W., Ripley B.D., Brady M., Smith S.M. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 2001, 14(6):1370-1386.
84. Zaki J., Davis J.I., Ochsner K.N. Overlapping activity in anterior insula during interoception and emotional experience. Neuroimage 2012, 62(1):493-499.
85. Zigmond A.S., Snaith R.P. The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica 1983, 67(6):361-370.