Amygdala response to explicit sad face stimuli at baseline predicts antidepressant treatment response to scopolamine in major depressive disorder

Psychiatry Research - Neuroimaging

Volumn 254, Issue , 2016, Pages 67-73

  Szczepanik, Joanna ^a   Nugent, Allison C ^a   Drevets, Wayne C ^b   Khanna, Ashish ^c   Zarate, Carlos A ^a   Furey, Maura L ^a,d  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b JANSSEN RESEARCH AND DEVELOPMENT   (United States)

^c BROOKLYN HOSPITAL CENTER   (United States)

^d JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

Amygdala; Functional magnetic resonance imaging (fMRI); Major depressive disorder; Rapid acting antidepressants; Scopolamine; Stimulus processing

Indexed keywords

ANTIDEPRESSANT AGENT; BIOLOGICAL MARKER; SCOPOLAMINE; MUSCARINIC RECEPTOR BLOCKING AGENT; SCOPOLAMINE BROMIDE;

ADULT; AMYGDALA; ARTICLE; BOLD SIGNAL; CHOLINERGIC ACTIVITY; CLINICAL ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; EMOTION; FACIAL RECOGNITION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MAJOR DEPRESSION; MALE; NERVE POTENTIAL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REACTION TIME; SADNESS; STIMULUS RESPONSE; TASK PERFORMANCE; TREATMENT OUTCOME; TREATMENT RESPONSE; DEPRESSIVE DISORDER, MAJOR; FACIAL EXPRESSION; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY;

ADULT; AMYGDALA; BIOMARKERS; DEPRESSIVE DISORDER, MAJOR; FACIAL EXPRESSION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MUSCARINIC ANTAGONISTS; OUTCOME ASSESSMENT (HEALTH CARE); SCOPOLAMINE HYDROBROMIDE;

EID: 84977098340     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2016.06.005     Document Type: Article

References (53)

1. Arnone, D., McKie, S., Elliott, R., Thomas, E.J., Downey, D., Juhasz, G., Williams, S.R., Deakin, J.F., Anderson, I.M., Increased amygdala responses to sad but not fearful faces in major depression: relation to mood state and pharmacological treatment. Am. J. Psychiatry 169:8 (2012), 841–850.
2. Bentley, P., Vuilleumier, P., Thiel, C.M., Driver, J., Dolan, R.J., Cholinergic enhancement modulates neural correlates of selective attention and emotional processing. NeuroImage 20:1 (2003), 58–70.
3. Boubela, R.N., Kalcher, K., Huf, W., Seidel, E.-M., Derntl, B., Pezawas, L., Našel, C., Moser, E., fMRI measurements of amygdala activation are confounded by stimulus correlated signal fluctuation in nearby veins draining distant brain regions. Sci. Rep., 5, 2015, 10499.
4. Breitenstein, B., Scheuer, S., Holsboer, F., Are there meaningful biomarkers of treatment response for depression?. Drug Discov. Today 19:5 (2014), 539–561.
5. Canli, T., Cooney, R.E., Goldin, P., Shah, M., Sivers, H., Thomason, M.E., Whitfield-Gabrieli, S., Gabrieli, J.D., Gotlib, I.H., Amygdala reactivity to emotional faces predicts improvement in major depression. NeuroReport 16:12 (2005), 1267–1270.
6. Cox, R.W., AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29:3 (1996), 162–173.
7. Desikan, R.S., Segonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., Buckner, R.L., Dale, A.M., Maguire, R.P., Hyman, B.T., Albert, M.S., Killiany, R.J., An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:3 (2006), 968–980.
8. Dilsaver, S.C., Pathophysiology of “cholinoceptor supersensitivity” in affective disorders. Biol. Psychiatry 21:8–9 (1986), 813–829.
9. Drevets, W.C., Bogers, W., Raichle, M.E., Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism. Eur. Neuropsychopharmacol. 12:6 (2002), 527–544.
10. Drevets, W.C., Furey, M.L., Replication of scopolamine's antidepressant efficacy in major depressive disorder: a randomized, placebo-controlled clinical trial. Biol. Psychiatry 67:5 (2010), 432–438.
11. Elliott, R., Rubinsztein, J.S., Sahakian, B.J., Dolan, R.J., The neural basis of mood-congruent processing biases in depression. Arch. Gen. Psychiatry 59:7 (2002), 597–604.
12. Ellis, J.S., Zarate, C.A. Jr., Luckenbaugh, D.A., Furey, M.L., Antidepressant treatment history as a predictor of response to scopolamine: clinical implications. J. Affect. Disord. 162 (2014), 39–42.
13. Erickson, K., Drevets, W.C., Clark, L., Cannon, D.M., Bain, E.E., Zarate, C.A., Charney, D.S., Sahakian, B.J., Mood-congruent bias in affective Go/No-Go performance of unmedicated patients with major depressive disorder. Am. J. Psychiatry 162:11 (2005), 2171–2173.
14. Fales, C.L., Barch, D.M., Rundle, M.M., Mintun, M.A., Snyder, A.Z., Cohen, J.D., Mathews, J., Sheline, Y.I., Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biol. Psychiatry 63:4 (2008), 377–384.
15. Ferrari, A.J., Somerville, A.J., Baxter, A.J., Norman, R., Patten, S.B., Vos, T., Whiteford, H.A., Global variation in the prevalence and incidence of major depressive disorder: a systematic review of the epidemiological literature. Psychol. Med. 43:03 (2013), 471–481.
16. First, M.B., Spitzer, R.L., Gibbon, M., Williams, J.B.W., Structured Clinical Interview for DSM-IV. 1997, American Psychiatric Press, Washington, DC.
17. Fu, C.H., Williams, S.C., Cleare, A.J., Brammer, M.J., Walsh, N.D., Kim, J., Andrew, C.M., Pich, E.M., Williams, P.M., Reed, L.J., Mitterschiffthaler, M.T., Suckling, J., Bullmore, E.T., Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. Arch. Gen. Psychiatry 61 (2004), 877–889.
18. Furey, M.L., The prominent role of stimulus processing: cholinergic function and dysfunction in cognition. Curr. Opin. Neurol. 24:4 (2011), 364–370.
19. Furey, M.L., Drevets, W.C., Antidepressant efficacy of the antimuscarinic drug scopolamine: a randomized, placebo-controlled clinical trial. Arch. Gen. Psychiatry 63:10 (2006), 1121–1129.
20. Furey, M.L., Drevets, W.C., Szczepanik, J., Khanna, A., Nugent, A., Zarate, C.A., Pre-treatment differences in BOLD response to emotional faces correlate with antidepressant response to scopolamine. Int. J. Neuropsychopharmacol., 2015, 28 (Epub ahead of print).
21. Furey, M.L., Nugent, A.C., Speer, A.M., Luckenbaugh, D.A., Hoffman, E.M., Frankel, E., Drevets, W.C., Zarate, C.A. Jr., Baseline mood-state measures as predictors of antidepressant response to scopolamine. Psychiatry Res. 196:1 (2012), 62–67.
22. Furey, M.L., Pietrini, P., Haxby, J.V., Drevets, W.C., Selective effects of cholinergic modulation on task performance during selective attention. Neuropsychopharmacology 33:4 (2008), 913–923.
23. Furey, M.L., Ricciardi, E., Schapiro, M.B., Rapoport, S.I., Pietrini, P., Cholinergic enhancement eliminates modulation of neural activity by task difficulty in the prefrontal cortex during working memory. J. Cogn. Neurosci. 20:7 (2008), 1342–1353.
24. Gorka, A.X., Knodt, A.R., Hariri, A.R., Basal forebrain moderates the magnitude of task-dependent amygdala functional connectivity. Soc. Cogn. Affect. Neurosci. 10 (2015), 501–507.
25. Gotlib, I.H., Krasnoperova, E., Yue, D.N., Joormann, J., Attentional biases for negative interpersonal stimuli in clinical depression. J. Abnorm. Psychol. 113 (2004), 127–135.
26. Harmer, C.J., O'Sullivan, U., Favaron, E., Massey-Chase, R., Ayres, R., Reinecke, A., Goodwin, G.M., Cowen, P.J., Effect of acute antidepressant administration on negative affective bias in depressed patients. Am. J. Psychiatry 166:10 (2009), 1178–1184.
27. Himmelheber, A.M., Sarter, M., Bruno, J.P., The effects of manipulations of attentional demand on cortical acetylcholine release. Brain Res. Cogn. Brain Res. 12:3 (2001), 353–370.
28. Insel, T.R., Translating scientific opportunity into public health impact: a strategic plan for research on mental illness. Arch. Gen. Psychiatry 66:2 (2009), 128–133.
29. Janowsky, D.S., el-Yousef, M.K., Davis, J.M., Acetylcholine and depression. Psychosom. Med. 36:3 (1974), 248–257.
30. Janowsky, D.S., el-Yousef, M.K., Davis, J.M., Sekerke, H.J., A cholinergic-adrenergic hypothesis of mania and depression. Lancet 2:7778 (1972), 632–635.
31. Johnstone, T., Somerville, L.H., Alexander, A.L., Oakes, T.R., Davidson, R.J., Kalin, N.H., Whalen, P.J., Stability of amygdala BOLD response to fearful faces over multiple scan sessions. NeuroImage 25:4 (2005), 1112–1123.
32. Kessler, R.C., The costs of depression. Psychiatr. Clin. N. Am. 35:1 (2012), 1–14.
33. Luyten, P., Blatt, S.J., Van Houdenhove, B., Corveleyn, J., Depression research and treatment: are we skating to where the puck is going to be?. Clin. Psychol. Rev. 26:8 (2006), 985–999.
34. Machado-Vieira, R., Salvadore, G., Diazgranados, N., Zarate, C.A. Jr., Ketamine and the next generation of antidepressants with a rapid onset of action. Pharmacol. Ther. 123:2 (2009), 143–150.
35. Mesulam, M.M., Cholinergic circuitry of the human nucleus basalis and its fate in Alzheimer's disease. J. Comp. Neurol. 521:18 (2013), 4124–4144.
36. Mesulam, M.M., Geula, C., Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: Observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J. Comp. Neurol. 275:2 (1988), 216–240.
37. Miller, D.B., O'Callaghan, J.P., Personalized medicine in major depressive disorder–opportunities and pitfalls. Metabolism 62:Suppl 1 (2013), S34–S39.
38. Montgomery, S.A., Asberg, M., A new depression scale designed to be sensitive to change. Br. J. Psychiatry 134:4 (1979), 382–389.
39. Overstreet, D.H., Russell, R.W., Crocker, A.D., Gillin, J.C., Janowsky, D.S., Genetic and pharmacological models of cholinergic supersensitivity and affective disorders. Experientia 44:6 (1988), 465–472.
40. Pessoa, L., Adolphs, R., Emotion processing and the amygdala: from a ‘low road’ to ‘many roads’ of evaluating biological significance. Nat. Rev. Neurosci. 11:11 (2010), 773–782.
41. Phelps, E.A., Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol. 57 (2006), 27–53.
42. Safer, D.J., Allen, R.P., The central effects of scopolamine in man. Biol. Psychiatry 3:4 (1971), 347–355.
43. Schmidt, H.D., Shelton, R.C., Duman, R.S., Functional biomarkers of depression: diagnosis, treatment, and pathophysiology. Neuropsychopharmacology 36:12 (2011), 2375–2394.
44. Sheline, Y.I., Barch, D.M., Donnelly, J.M., Ollinger, J.M., Snyder, A.Z., Mintun, M.A., Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol. Psychiatry 50:9 (2001), 651–658.
45. Siegle, G.J., Carter, C.S., Thase, M.E., Use of fMRI to predict recovery from unipolar depression with cognitive behavior therapy. Am. J. Psychiatry 163:4 (2006), 735–738.
46. Simon, G.E., Perlis, R.H., Personalized medicine for depression: can we match patients with treatments?. Am. J. Psychiatry 167:12 (2010), 1445–1455.
47. Surguladze, S.A., Young, A.W., Senior, C., Brébion, G., Travis, M.J., Phillips, M.L., Recognition accuracy and response bias to happy and sad facial expressions in patients with major depression. Neuropsychology 18 (2004), 212–218.
48. Talairach, J., Tournoux, P., Co-Planar Stereotaxic Atlas of the Human Brain. 1988, Georg Thieme Verlag, Stuttgart, Germany.
49. Victor, T.A., Furey, M.L., Fromm, S.J., Bellgowan, P.S., Ohman, A., Drevets, W.C., The extended functional neuroanatomy of emotional processing biases for masked faces in major depressive disorder. PLoS One, 7(10), 2012, e46439.
50. Victor, T.A., Furey, M.L., Fromm, S.J., Ohman, A., Drevets, W.C., Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Arch. Gen. Psychiatry 67:11 (2010), 1128–1138.
51. Whalen, P.J., Shin, L.M., Somerville, L.H., McLean, A.A., Kim, H., Functional neuroimaging studies of the amygdala in depression. Semin. Clin. Neuropsychiatry 7:4 (2002), 234–242.
52. Williams, L.M., Korgaonkar, M.S., Song, Y.C., Paton, R., Eagles, S., Goldstein-Piekarski, A., Grieve, S.M., Harris, A.W., Usherwood, T., Etkin, A., Amygdala reactivity to emotional faces in the prediction of general and medication-specific responses to antidepressant treatment in the randomized iSPOT-D trial. Neuropsychopharmacology 40 (2015), 2398–2408.
53. Zarate, C.A., Mathews, D.C., Furey, M.L., Human biomarkers of rapid antidepressant effects. Biol. Psychiatry 73:12 (2013), 1142–1155.