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Effects of electroconvulsive therapy on amygdala function in major depression – a longitudinal functional magnetic resonance imaging study

Published online by Cambridge University Press:  11 April 2017

R. Redlich*
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
C. Bürger
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
K. Dohm
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
D. Grotegerd
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
N. Opel
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
D. Zaremba
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
S. Meinert
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
K. Förster
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
J. Repple
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
R. Schnelle
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
C. Wagenknecht
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
M. Zavorotnyy
Affiliation:
Department of Psychiatry, University of Marburg, Marburg, Germany
W. Heindel
Affiliation:
Department of Clinical Radiology, University of Münster, Münster, Germany
H. Kugel
Affiliation:
Department of Clinical Radiology, University of Münster, Münster, Germany
M. Gerbaulet
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
J. Alferink
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany Cells-in-Motion Cluster of Excellence, University of Münster, Münster, Germany
V. Arolt
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
P. Zwanzger
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany Inn-Salzach Hospital, Wasserburg am Inn, Germany Ludwig-Maximilians-University Munich, Munich, Germany
U. Dannlowski
Affiliation:
Department of Psychiatry, University of Münster, Münster, Germany
*
*Address for correspondence: R. Redlich, Ph.D., Department of Psychiatry, University of Münster, Albert-Schweitzer-Campus 1, A9, 48149 Münster, Germany. (Email: r.redlich@uni-muenster.de)

Abstract

Background

Electroconvulsive therapy (ECT) is one of the most effective treatments for severe depression. However, little is known regarding brain functional processes mediating ECT effects.

Method

In a non-randomized prospective study, functional magnetic resonance imaging data during the automatic processing of subliminally presented emotional faces were obtained twice, about 6 weeks apart, in patients with major depressive disorder (MDD) before and after treatment with ECT (ECT, n = 24). Additionally, a control sample of MDD patients treated solely with pharmacotherapy (MED, n = 23) and a healthy control sample (HC, n = 22) were obtained.

Results

Before therapy, both patient groups equally showed elevated amygdala reactivity to sad faces compared with HC. After treatment, a decrease in amygdala activity to negative stimuli was discerned in both patient samples indicating a normalization of amygdala function, suggesting mechanisms potentially unspecific for ECT. Moreover, a decrease in amygdala activity to sad faces was associated with symptomatic improvements in the ECT sample (rspearman = −0.48, p = 0.044), and by tendency also for the MED sample (rspearman = −0.38, p = 0.098). However, we did not find any significant association between pre-treatment amygdala function to emotional stimuli and individual symptom improvement, neither for the ECT sample, nor for the MED sample.

Conclusions

In sum, the present study provides first results regarding functional changes in emotion processing due to ECT treatment using a longitudinal design, thus validating and extending our knowledge gained from previous treatment studies. A limitation was that ECT patients received concurrent medication treatment.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2017 

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References

Abbott, CC, Jones, T, Lemke, NT, Gallegos, P, McClintock, SM, Mayer, AR, Bustillo, J, Calhoun, VD (2014). Hippocampal structural and functional changes associated with electroconvulsive therapy response. Translational Psychiatry 4, e483.CrossRefGoogle ScholarPubMed
Anand, A, Li, Y, Wang, Y, Gardner, K, Lowe, MJ (2007). Reciprocal effects of antidepressant treatment on activity and connectivity of the mood regulating circuit: an fMRI study. Journal of Neuropsychiatry and Clinical Neurosciences 19, 274282.CrossRefGoogle ScholarPubMed
Argyelan, M, Lencz, T, Kaliora, S, Sarpal, DK, Weissman, N, Kingsley, PB, Malhotra, AK, Petrides, G (2016). Subgenual cingulate cortical activity predicts the efficacy of electroconvulsive therapy. Translational Psychiatry 6, e789.CrossRefGoogle ScholarPubMed
Bogod, NM, Sinden, M, Woo, C, Defreitas, VG, Torres, IJ, Howard, AK, Ilcewicz-Klimek, MI, Honey, CR, Yatham, LN, Lam, RW (2014). Long-term neuropsychological safety of subgenual cingulate gyrus deep brain stimulation for treatment-resistant depression. Journal of Neuropsychiatry and Clinical Neurosciences 26, 126133.CrossRefGoogle ScholarPubMed
Bouckaert, F, De Winter, FL, Emsell, L, Dols, A, Rhebergen, D, Wampers, M, Sunaert, S, Stek, ML, Sienaert, P, Vandenbulcke, M (2016). Grey matter volume increase following electroconvulsive therapy in patients with late life depression: a longitudinal MRI study. Journal of Psychiatry and Neuroscience 41, 105114.CrossRefGoogle ScholarPubMed
Canli, T, Cooney, RE, Goldin, P, Shah, M, Sivers, H, Thomason, ME, Whitfield-Gabrieli, S, Gabrieli, JDE, Gotlib, IH (2005). Amygdala reactivity to emotional faces predicts improvement in major depression. Neuroreport 16, 12671270.CrossRefGoogle ScholarPubMed
Dannlowski, U, Grabe, HJ, Wittfeld, K, Klaus, J, Konrad, C, Grotegerd, D, Redlich, R, Suslow, T, Opel, N, Ohrmann, P, Bauer, J, Zwanzger, P, Laeger, I, Hohoff, C, Arolt, V, Heindel, W, Deppe, M, Domschke, K, Hegenscheid, K, Völzke, H, Stacey, D, Meyer Zu Schwabedissen, H, Kugel, H, Baune, BT (2015). Multimodal imaging of a tescalcin (TESC)-regulating polymorphism (rs7294919)-specific effects on hippocampal gray matter structure. Molecular Psychiatry 20, 398404.CrossRefGoogle ScholarPubMed
Dannlowski, U, Konrad, C, Kugel, H, Zwitserlood, P, Domschke, K, Schöning, S, Ohrmann, P, Bauer, J, Pyka, M, Hohoff, C, Zhang, W, Baune, BT, Heindel, W, Arolt, V, Suslow, T (2010). Emotion specific modulation of automatic amygdala responses by 5-HTTLPR genotype. NeuroImage 53, 893898.CrossRefGoogle ScholarPubMed
Dannlowski, U, Kugel, H, Huber, F, Stuhrmann, A, Redlich, R, Grotegerd, D, Dohm, K, Sehlmeyer, C, Konrad, C, Baune, BT, Arolt, V, Heindel, W, Zwitserlood, P, Suslow, T (2013). Childhood maltreatment is associated with an automatic negative emotion processing bias in the amygdala. Human Brain Mapping 34, 28992909.CrossRefGoogle ScholarPubMed
De Raedt, R, Leyman, L, Baeken, C, Van Schuerbeek, P, Luypaert, R, Vanderhasselt, M-A, Dannlowski, U (2010). Neurocognitive effects of HF-rTMS over the dorsolateral prefrontal cortex on the attentional processing of emotional information in healthy women: an event-related fMRI study. Biological Psychology 85, 487495.CrossRefGoogle ScholarPubMed
Dukart, J, Regen, F, Kherif, F, Colla, M, Bajbouj, M, Heuser, I (2014). Electroconvulsive therapy-induced brain plasticity determines therapeutic outcome in mood disorders. PNAS 111, 11561161.CrossRefGoogle ScholarPubMed
Ekman, P, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Forman, SD, Cohen, JD, Fitzgerald, M, Eddy, WF, Mintun, MA, Noll, DC (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance Medicine 33, 636647.CrossRefGoogle ScholarPubMed
Fu, CHY, Williams, SCR, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J, Andrew, C, Pich, EM, Williams, PM, Reed, LJ, Mitterschiffthaler, MT, Suckling, J, Bullmore, ET (2004). Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. Archives of General Psychiatry 61, 877889.CrossRefGoogle ScholarPubMed
Groenewold, NA, Opmeer, EM, de Jonge, P, Aleman, A, Costafreda, SG (2013). Emotional valence modulates brain functional abnormalities in depression: evidence from a meta-analysis of fMRI studies. Neuroscience and Biobehavioral Reviews 37, 152163.CrossRefGoogle ScholarPubMed
Grotegerd, D, Stuhrmann, A, Kugel, H, Schmidt, S, Redlich, R, Zwanzger, P, Rauch, AV, Heindel, W, Zwitserlood, P, Arolt, V, Suslow, T, Dannlowski, U (2014). Amygdala excitability to subliminally presented emotional faces distinguishes unipolar and bipolar depression – an fMRI and pattern classification study. Human Brain Mapping 35, 29953007.CrossRefGoogle ScholarPubMed
Hamilton, JP, Etkin, A, Furman, DJ, Lemus, MG, Johnson, RF, Gotlib, IH (2012). Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. American Journal of Psychiatry 169, 693703.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 5663.CrossRefGoogle ScholarPubMed
Harmer, CJ, Goodwin, GM, Cowen, PJ (2009). Why do antidepressants take so long to work? A cognitive neuropsychological model of antidepressant drug action. British Journal of Psychiatry: the Journal of Mental Science 195, 102108.CrossRefGoogle Scholar
Hautzinger, M, Bailer, M, Worall, H, Keller, F (1994). Beck Depressions-Inventar (BDI). Testhandbuch. Hans Huber: Bern.Google Scholar
Joormann, J, Cooney, RE, Henry, ML, Gotlib, IH (2011). Neural correlates of automatic mood regulation in girls at high risk for depression. Journal of Abnormal Psychology 121, 6172.CrossRefGoogle ScholarPubMed
Jorgensen, A, Magnusson, P, Hanson, LG, Kirkegaard, T, Benveniste, H, Lee, H, Svarer, C, Mikkelsen, JD, Fink-Jensen, A, Knudsen, GM, Paulson, OB, Bolwig, TG, Jorgensen, MB (2015). Regional brain volumes, diffusivity, and metabolite changes after electroconvulsive therapy for severe depression. Acta Psychiatrica Scandinavica 133, 154164.CrossRefGoogle ScholarPubMed
Joshi, SH, Espinoza, RT, Pirnia, T, Shi, J, Wang, Y, Ayers, B, Leaver, A, Woods, RP, Narr, KL (2016). Structural plasticity of the hippocampus and amygdala induced by electroconvulsive therapy in major depression. Biological Psychiatry 79, 282292.CrossRefGoogle ScholarPubMed
Kho, KH, van Vreeswijk, MF, Simpson, S, Zwinderman, AH (2003). A meta-analysis of electroconvulsive therapy efficacy in depression. Journal of ECT 19, 139147.CrossRefGoogle ScholarPubMed
Kuhs, H (1995). [Stages of treatment resistance in depressive disorders, defined after somatotherapeutic methods]. Der Nervenarzt 66, 561567.Google ScholarPubMed
Leaver, AM, Espinoza, R, Pirnia, T, Joshi, SH, Woods, RP, Narr, KL (2016). Modulation of intrinsic brain activity by electroconvulsive therapy in major depression. Biological Psychiatry 1, 7786.Google ScholarPubMed
Liu, Y, Du, L, Li, Y, Liu, H, Zhao, W, Liu, D, Zeng, J, Li, X, Fu, Y, Qiu, H, Li, X, Qiu, T, Hu, H, Meng, H, Luo, Q (2015). Antidepressant effects of electroconvulsive therapy correlate with subgenual anterior cingulate activity and connectivity in depression. Medicine 94, e2033.CrossRefGoogle ScholarPubMed
Nickl-Jockschat, T, Palomero Gallagher, N, Kumar, V, Hoffstaedter, F, Brügmann, E, Habel, U, Eickhoff, SB, Grözinger, M (2016). Are morphological changes necessary to mediate the therapeutic effects of electroconvulsive therapy? European Archives of Psychiatry and Clinical Neuroscience 266, 261267.CrossRefGoogle ScholarPubMed
Njau, S, Joshi, SH, Espinoza, R, Leaver, AM, Vasavada, M, Marquina, A, Woods, RP, Narr, KL (2016). Neurochemical correlates of rapid treatment response to electroconvulsive therapy in patients with major depression. Journal of Psychiatry and Neuroscience 41, 150177.Google Scholar
Norbury, R, Taylor, MJ, Selvaraj, S, Murphy, SE, Harmer, CJ, Cowen, PJ (2009). Short-term antidepressant treatment modulates amygdala response to happy faces. Psychopharmacology 206, 197204.CrossRefGoogle ScholarPubMed
Opel, N, Redlich, R, Grotegerd, D, Dohm, K, Haupenthal, C, Heindel, W, Kugel, H, Arolt, V, Dannlowski, U (2015). Enhanced neural responsiveness to reward associated with obesity in the absence of food-related stimuli. Human Brain Mapping 36, 23302337.CrossRefGoogle ScholarPubMed
Redlich, R, Almeida, JRC, Grotegerd, D, Opel, N, Kugel, H, Heindel, W, Arolt, V, Phillips, ML, Dannlowski, U (2014). Brain morphometric biomarkers distinguishing unipolar and bipolar depression: a voxel-based morphometry-pattern classification approach. JAMA Psychiatry 71, 12221230.CrossRefGoogle ScholarPubMed
Redlich, R, Dohm, K, Grotegerd, D, Opel, N, Zwitserlood, P, Heindel, W, Arolt, V, Kugel, H, Dannlowski, U (2015 a). Reward processing in unipolar and bipolar depression: a functional MRI study. Neuropsychopharmacology 40, 26232631.CrossRefGoogle ScholarPubMed
Redlich, R, Grotegerd, D, Opel, N, Kaufmann, C, Zwitserlood, P, Kugel, H, Heindel, W, Donges, US, Suslow, T, Arolt, V, Dannlowski, U (2015 b). Are you gonna leave me? Separation anxiety is associated with increased amygdala responsiveness and volume. Social Cognitive and Affective Neuroscience 10, 278284.CrossRefGoogle ScholarPubMed
Redlich, R, Opel, N, Grotegerd, D, Dohm, K, Zaremba, D, Bürger, C, Münker, S, Mühlmann, L, Wahl, P, Heindel, W, Arolt, V, Alferink, J, Zwanzger, P, Zavorotnyy, M, Kugel, H, Dannlowski, U (2016). Prediction of individual response to electroconvulsive therapy via machine learning on structural magnetic resonance imaging data. JAMA Psychiatry 73, 557564.CrossRefGoogle ScholarPubMed
Redlich, R, Stacey, D, Opel, N, Grotegerd, D, Dohm, K, Kugel, H, Heindel, W, Arolt, V, Baune, BT, Dannlowski, U (2015 c). Evidence of an IFN-γ by early life stress interaction in the regulation of amygdala reactivity to emotional stimuli. Psychoneuroendocrinology 62, 166173.CrossRefGoogle ScholarPubMed
Salvadore, G, Cornwell, BR, Colon-Rosario, V, Coppola, R, Grillon, C, Zarate, CA, Manji, HK (2009). Increased anterior cingulate cortical activity in response to fearful faces: a neurophysiological biomarker that predicts rapid antidepressant response to ketamine. Biological Psychiatry 65, 289295.CrossRefGoogle Scholar
Sheline, YI, Barch, DM, Donnelly, JM, Ollinger, JM, Snyder, AZ, Mintun, MA (2001). Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biological Psychiatry 50, 651658.CrossRefGoogle ScholarPubMed
Siegle, GJ, Carter, CS, Thase, ME (2006). Use of fMRI to predict recovery from unipolar depression with cognitive behavior therapy. American Journal of Psychiatry 163, 735738.CrossRefGoogle ScholarPubMed
Siegle, GJ, Thompson, WK, Carter, CS, Steinhauer, SR, Thase, ME (2007). Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biological Psychiatry 61, 198209.CrossRefGoogle ScholarPubMed
Stuhrmann, A, Dohm, K, Kugel, H, Zwanzger, P, Redlich, R, Grotegerd, D, Rauch, AV, Arolt, V, Heindel, W, Suslow, T, Zwitserlood, P, Dannlowski, U (2013). Mood-congruent amygdala responses to subliminally presented facial expressions in major depression: associations with anhedonia. Journal of Psychiatry and Neuroscience 37, 249258.CrossRefGoogle Scholar
Suslow, T, Konrad, C, Kugel, H, Rumstadt, D, Zwitserlood, P, Schöning, S, Ohrmann, P, Bauer, J, Pyka, M, Kersting, A, Arolt, V, Heindel, W, Dannlowski, U (2010). Automatic mood-congruent amygdala responses to masked facial expressions in major depression. Biological Psychiatry 67, 155160.CrossRefGoogle ScholarPubMed
Suslow, T, Kugel, H, Ohrmann, P, Stuhrmann, A, Grotegerd, D, Redlich, R, Bauer, J, Dannlowski, U (2013). Neural correlates of affective priming effects based on masked facial emotion: an fMRI study. Psychiatry Research 211, 239245.CrossRefGoogle ScholarPubMed
Taghva, AS, Malone, DA, Rezai, AR (2013). Deep brain stimulation for treatment-resistant depression. World Neurosurgery 80, S27.e17S27.e24.CrossRefGoogle ScholarPubMed
Tendolkar, I, van Beek, M, van Oostrom, I, Mulder, M, Janzing, J, Voshaar, RO, van Eijndhoven, P (2013). Electroconvulsive therapy increases hippocampal and amygdala volume in therapy refractory depression: a longitudinal pilot study. Psychiatry Research 214, 197203.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273289.CrossRefGoogle ScholarPubMed
van Harmelen, A-L, van Tol, M-J, Demenescu, LR, van der Wee, NJA, Veltman, DJ, Aleman, A, van Buchem, MA, Spinhoven, P, Penninx, B, Elzinga, BM (2013). Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience 8, 362369.CrossRefGoogle ScholarPubMed
van Waarde, JA, Scholte, HS, van Oudheusden, LJB, Verwey, B, Denys, D, van Wingen, GA (2015). A functional MRI marker may predict the outcome of electroconvulsive therapy in severe and treatment-resistant depression. Molecular Psychiatry 20, 609614.CrossRefGoogle ScholarPubMed
Victor, TA, Furey, ML, Fromm, SJ, Ohman, A, Drevets, WC (2010). Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Archives of General Psychiatry 67, 11281138.CrossRefGoogle ScholarPubMed
Williams, LM, Korgaonkar, MS, Song, YC, Paton, R, Eagles, S, Goldstein-Piekarski, A, Grieve, SM, Harris, AW, Usherwood, T, Etkin, A (2015). 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, 23982408.CrossRefGoogle ScholarPubMed
Wittchen, H-U, Wunderlich, U, Gruschwitz, S, Zaudig, M (1997). Strukturiertes Klinisches Interview für DSM-IV. Hogrefe: Goettingen.Google Scholar