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Glucocorticoids Enhance Extinction-Based Psychotherapy

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Glucocorticoids Enhance Extinction-Based Psychotherapy Glucocorticoids enhance extinction-based SEE COMMENTARY psychotherapy Dominique J.-F. de Quervaina,b,1, Dorothée Bentza, Tanja Michaelc, Olivia C. Boltd, Brenda K. Wiederholde,f, Jürgen Margrafg, and Frank H. Wilhelmh aDivision of Cognitive Neuroscience, Department of Psychology, and bPsychiatric University Clinics, University of Basel, 4055 Basel, Switzerland; cDepartment of Clinical Psychology and Psychotherapy, University of Saarbrücken, 66123 Saarbrücken, Germany; dDepartment of Psychology, King’s College London Institute of Psychiatry, Denmark Hill, London SE5 8AF, United Kingdom; eVirtual Reality Medical Institute, 1150 Woluwe-Saint-Pierre, Belgium; fVirtual Reality Medical Center, San Diego, CA 92121; gDepartment of Clinical Psychology and Psychotherapy, Ruhr-Universität Bochum, 44301 Bochum, Germany; and hDepartment of Clinical Psychology, Psychotherapy, and Health Psychology, University of Salzburg, 5020 Salzburg, Austria Edited* by James L. McGaugh, University of California, Irvine, CA, and approved December 20, 2010 (received for review December 6, 2010) Behavioral exposure therapy of anxiety disorders is believed to rely Mental Disorders, Fourth Edition (DSM-IV) were treated with on fear extinction. Because preclinical studies have shown that glu- three sessions of exposure therapy using virtual exposure to heights. cocorticoids can promote extinction processes, we aimed at inves- Virtual reality (VR) exposure therapy has proven effective in the tigating whether the administration of these hormones might be treatment of patients with acrophobia (30–34) and is ideal for useful in enhancing exposure therapy. In a randomized, double- clinical research, as it allows identical exposure of all patients and blind, placebo-controlled study, 40 patients with specific phobia avoids unpredicted events that may occur in real environments for heights were treated with three sessions of exposure therapy (35). Cortisol (20 mg) or placebo was administered orally 1 h before using virtual reality exposure to heights. Cortisol (20 mg) or placebo each of the treatment sessions. Subjects returned for a posttreat- was administered orally 1 h before each of the treatment sessions. ment assessment 3–5 d after the last treatment session and for a Subjects returned for a posttreatment assessment 3–5 d after the last follow-up assessment after 1 mo (28–35 d after last treatment ses- treatment session and for a follow-up assessment after 1 mo. Adding sion). Symptom severity was assessed with fear of heights ques- cortisol to exposure therapy resulted in a significantly greater reduc- tionnaires and subjective ratings of acute fear in height situations tion in fear of heights as measured with the acrophobia question- at pretreatment, posttreatment, and follow-up. Furthermore, we naire (AQ) both at posttreatment and at follow-up, compared with measured skin conductance response, which has been shown to be placebo. Furthermore, subjects receiving cortisol showed a signifi- reduced after successful fear extinction (36). cantly greater reduction in acute anxiety during virtual exposure to a phobic situation at posttreatment and a significantly smaller expo- Results sure-induced increase in skin conductance level at follow-up. The The cortisol group and the placebo group consisted each of 20 present findings indicate that the administration of cortisol can en- patients (11 males, 9 females). The groups did not differ signifi- hance extinction-based psychotherapy. cantly in demographic and clinical characteristics, or in any of the baseline measurements taken before treatment (Table 1). On all memory | retrieval | consolidation sessions with pharmacological treatment (i.e., treatment sessions 1–3), subjects who had received cortisol had significantly higher hobic disorders can be characterized as disorders involving salivary cortisol concentrations before (P ≤ 0.001) and after (P ≤ Pdisturbed emotional learning and memory resulting in an en- 0.007) VR exposure than subjects who had received placebo (Ta- hanced fear response. A central mechanism in the pathogenesis of ble S1). No differences in baseline salivary cortisol concentrations anxiety disorders is associative learning or conditioning that leads were found between the treatment groups on any of the study days to formation of a fear memory (1–5). In phobic individuals, ex- (P ≥ 0.332). None of the patients reported adverse effects due to posure to a phobic stimulus almost invariably provokes retrieval substance administration. of stimulus-associated fear memory, which leads to the fear re- sponse (6–9). Exposure-based behavioral therapy of phobia is Effects of VR Exposure. We found a significant reduction of fear as thought to rely on extinction of these fear responses (10–13). Ex- measured with the acrophobia questionnaire (AQ) from pre- tinction occurs when conditioned responding to a stimulus de- treatment assessment (59.3 ± 2.8; mean ± SE) to posttreatment creases when the reinforcer is omitted (12, 14). Accordingly, fear assessment (35.7 ± 2.6; F1,35 =18.135;P < 0.001), and follow-up reduction induced by exposure therapy is the result of decrements (30.1 ± 2.8; F1,35 = 18.636; P < 0.001). The controlled effect size in the conditioned response over successive extinction trials. Ex- from pretreatment to posttreatment assessment was d = 1.3 and NEUROSCIENCE tinction leads to the formation of an alternative set of nonfearful from pretreatment to follow-up d = 1.6. Also in the danger expec- memory associations (extinction memory) that competes with, but tancy scale (DES) fear symptoms decreased from pretreatment does not erase original fear memory associations (14, 15). Con- (18.1 ± 0.6) to posttreatment (14.8 ± 0.7; F1,34 = 17.828; P < 0.001) sidering the importance of extinction learning for exposure ther- and follow-up (12.8 ± 0.6; F1,35 = 15.926; P < 0.001). No significant apy, pharmacological interventions aimed at enhancing extinction processes are promising approaches to enhance exposure therapy, – as it has been demonstrated with D-cycloserine (16 18). Author contributions: D.J.-F.d.Q., D.B., T.M., O.C.B., B.K.W., J.M., and F.H.W. designed Glucocorticoids (cortisol in humans, corticosterone in rodents) research; D.B. and O.C.B. performed research; D.J.-F.d.Q., D.B., T.M., O.C.B., B.K.W., are stress hormones released from the adrenal cortex and it has long J.M., and F.H.W. analyzed data; and D.J.-F.d.Q., D.B., T.M., O.C.B., B.K.W., J.M., and been recognized that they readily enter the brain and affect learning F.H.W. wrote the paper. and memory (19–24). Importantly, basic research studies in animals The authors declare no conflict of interest. and humans have shown that the mnemonic effects of glucocorti- *This Direct Submission article had a prearranged editor. coids can facilitate extinction processes (22, 25–29). Therefore, we Freely available online through the PNAS open access option. aimed at investigating whether the administration of these hor- See Commentary on page 6343. mones might be useful in enhancing exposure therapy. 1To whom correspondence should be addressed. E-mail: [email protected]. fi Forty patients with a diagnosis of speci c phobia for heights This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. according to criteria of the Diagnostic and Statistical Manual of 1073/pnas.1018214108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1018214108 PNAS | April 19, 2011 | vol. 108 | no. 16 | 6621–6625 Downloaded by guest on September 27, 2021 Table 1. Demographic and clinical characteristics and baseline measurements at pretreatment assessment Placebo group Cortisol group Significance, P Females/males 9/11 9/11 1.0 Age 40.2 (2.6) 42.8 (2.4) 0.461 BMI 26.4 (1.1) 25.6 (0.8) 0.558 Severity primary 5.4 (0.2) 5.4 (0.2) 0.874 diagnosis BDI total score 5.7 (1.2) 4.0 (1.0) 0.280 ASI total score 17.9 (1.8) 16.2 (1.8) 0.498 STAI trait total score 39.2 (1.8) 36.1 (1.4) 0.185 ITQ 5.3 (1.2) 4.2 (1.2) 0.524 AQ 58.9 (4.4) 58.4 (4.1) 0.927 ATHQ 41.5 (2.7) 39.3 (2.0) 0.517 DES 18.3 (1.0) 18.6 (0.9) 0.847 AES 20.1 (1.3) 20.0 (1.3) 0.962 Treatment credibility 23.6 (0.8) 22.8 (0.6) 0.462 SUD 48.8 (5.3) 49.4 (4.8) 0.940 BAT score 4.3 (0.4) 4.1 (0.4) 0.792 Fig. 1. Adding cortisol to VR exposure resulted in reductions of self-reported Data presented as mean (SEM). AES, anxiety expectancy scale; AQ, acro- fear of heights (measured with acrophobia questionnaire, range 0–120) at phobia questionnaire; ASI, anxiety sensitivity index; ATHQ, attitude toward posttreatment and at follow-up. VR exposure took place in three treatment heights questionnaire; BAT, behavioral avoidance test; BDI, Beck depression sessions between pretreatment and posttreatment assessment. Cortisol was inventory; BMI, body mass index; DES, danger expectancy scale; ITQ, immer- administered 1 h before each VR exposure session. Values are depicted sive tendencies questionnaire; STAI, state-trait anxiety inventory; SUD, sub- as mean and SEM. *P < 0.05 indicates significant difference between the jective units of discomfort. placebo- and cortisol group at a certain time point (see text for details). symptom decrease was observed with the anxiety expectancy scale Skin conductance. Due to technical reasons, skin conductance level (AES) and with the attitude toward heights questionnaire (ATHQ). (SCL) was only available from 25 subjects at posttreatment and No significant symptom change was measured from posttreatment from 20 subjects at follow-up. The treatment groups did not to follow-up in any of the questionnaires (AQ, DES, ATHQ, and differ significantly in demographic and clinical characteristics or AES) (P ≥ 0.127). Performance in the behavioral avoidance test in any of the baseline measurements taken before treatment (BAT) was enhanced from pretreatment (4.1 ± 0.3) to posttreat- (Tables S2 and S3).
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