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Longitudinal brain changes in MDD during emotional encoding: effects of presence and persistence of symptomatology

Published online by Cambridge University Press:  06 June 2019

Hui Ai
Affiliation:
Shenzhen Key Laboratory of Affective and Social Neuroscience, Center for Brain Disorders and Cognitive Sciences, Shenzhen University, Shenzhen, China Cognitive Neuroscience Center, Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, Groningen, The Netherlands
Esther M. Opmeer
Affiliation:
Cognitive Neuroscience Center, Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, Groningen, The Netherlands
Jan-Bernard C. Marsman
Affiliation:
Cognitive Neuroscience Center, Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, Groningen, The Netherlands
Dick J. Veltman
Affiliation:
Department of Psychiatry, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands Department of Anatomy and Neurosciences, Amsterdam Neuroscience, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
Nic J. A. van der Wee
Affiliation:
Department of Psychiatry, Leiden University Medical Center, Leiden, The Netherlands Leiden University, Leiden Institute for Brain and Cognition, Leiden, The Netherlands
André Aleman
Affiliation:
Shenzhen Key Laboratory of Affective and Social Neuroscience, Center for Brain Disorders and Cognitive Sciences, Shenzhen University, Shenzhen, China Cognitive Neuroscience Center, Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, Groningen, The Netherlands
Marie-José van Tol
Affiliation:
Cognitive Neuroscience Center, Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, Groningen, The Netherlands
Corresponding

Abstract

Background

The importance of the hippocampus and amygdala for disrupted emotional memory formation in depression is well-recognized, but it remains unclear whether functional abnormalities are state-dependent and whether they are affected by the persistence of depressive symptoms.

Methods

Thirty-nine patients with major depressive disorder and 28 healthy controls were included from the longitudinal functional magnetic resonance imaging (fMRI) sub-study of the Netherlands Study of Depression and Anxiety. Participants performed an emotional word-encoding and -recognition task during fMRI at baseline and 2-year follow-up measurement. At baseline, all patients were in a depressed state. We investigated state-dependency by relating changes in brain activation over time to changes in symptom severity. Furthermore, the effect of time spent with depressive symptoms in the 2-year interval was investigated.

Results

Symptom change was linearly associated with higher activation over time of the left anterior hippocampus extending to the amygdala during positive and negative word-encoding. Especially during positive word encoding, this effect was driven by symptomatic improvement. There was no effect of time spent with depression in the 2-year interval on change in brain activation. Results were independent of medication- and psychotherapy-use.

Conclusion

Using a longitudinal within-subjects design, we showed that hippocampal–amygdalar activation during emotional memory formation is related to depressive symptom severity but not persistence (i.e. time spent with depression or ‘load’), suggesting functional activation patterns in depression are not subject to functional ‘scarring’ although this hypothesis awaits future replication.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2019

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References

Ai, H, Opmeer, EM, Veltman, DJ, van der, W, Nic, JA, van Buchem, MA, Aleman, A and van Tol, M (2015) Brain activation during emotional memory processing associated with subsequent course of depression. Neuropsychopharmacology 40, 24542463.CrossRefGoogle ScholarPubMed
Anand, A, Li, Y, Wang, Y, Gardner, K and Lowe, MJ (2007) Reciprocal effects of antidepressant treatment on activity and connectivity of the mood regulating circuit: an FMRI study. The Journal of Neuropsychiatry and Clinical Neurosciences 19, 274282.CrossRefGoogle ScholarPubMed
Arnold, JF, Fitzgerald, DA, Fernández, G, Rijpkema, M, Rinck, M, Eling, PA, Becker, ES, Speckens, A and Tendolkar, I (2011) Rose or black-coloured glasses?: Altered neural processing of positive events during memory formation is a trait marker of depression. Journal of Affective Disorders 131, 214223.CrossRefGoogle ScholarPubMed
Arnone, D, McKie, S, Elliott, R, Juhasz, G, Thomas, E, Downey, D, Williams, S, Deakin, J and Anderson, I (2012 a) State-dependent changes in hippocampal grey matter in depression. Molecular Psychiatry 18, 12651272.10.1038/mp.2012.150CrossRefGoogle ScholarPubMed
Arnone, D, McKie, S, Elliott, R, Thomas, EJ, Downey, D, Juhasz, G, Williams, SR, Deakin, JW and Anderson, IM (2012 b) Increased amygdala responses to sad but not fearful faces in major depression: relation to mood state and pharmacological treatment. American Journal of Psychiatry 169, 841850.10.1176/appi.ajp.2012.11121774CrossRefGoogle Scholar
Beck, AT, Epstein, N, Brown, G and Steer, RA (1988) An inventory for measuring clinical anxiety: psychometric properties. Journal of Consulting and Clinical Psychology 56, 893.10.1037/0022-006X.56.6.893CrossRefGoogle ScholarPubMed
Bradley, BP and Mathews, A (1988) Memory bias in recovered clinical depressives. Cognition & Emotion 2, 235245.10.1080/02699938808410926CrossRefGoogle Scholar
Bremner, JD, Narayan, M, Anderson, ER, Staib, LH, Miller, HL and Charney, DS (2000) Hippocampal volume reduction in major depression. American Journal of Psychiatry 157, 115118.10.1176/ajp.157.1.115CrossRefGoogle ScholarPubMed
Calev, A, Korin, Y, Shapira, B, Kugelmass, S and Lerer, B (1986) Verbal and non-verbal recall by depressed and euthymic affective patients. Psychological Medicine 16, 789794.CrossRefGoogle ScholarPubMed
Chan, SW, Goodwin, GM and Harmer, CJ (2007) Highly neurotic never-depressed students have negative biases in information processing. Psychological Medicine 37, 12811291.10.1017/S0033291707000669CrossRefGoogle ScholarPubMed
Demenescu, L, Renken, R, Kortekaas, R, van Tol, M, Marsman, J, van Buchem, M, van der Wee, N, Veltman, D, den Boer, J and Aleman, A (2011) Neural correlates of perception of emotional facial expressions in out-patients with mild-to-moderate depression and anxiety. A multicenter fMRI study. Psychological Medicine 41, 22532264.10.1017/S0033291711000596CrossRefGoogle ScholarPubMed
Disner, SG, Beevers, CG, Haigh, EAP and Beck, AT (2011) Neural mechanisms of the cognitive model of depression. Nature Reviews Neuroscience 12, 467477.CrossRefGoogle ScholarPubMed
Dohm, K, Redlich, R, Zwitserlood, P and Dannlowski, U (2017) Trajectories of major depression disorders: a systematic review of longitudinal neuroimaging findings. The Australian and New Zealand Journal of Psychiatry 51, 441454.10.1177/0004867416661426CrossRefGoogle ScholarPubMed
Elliott, R, Zahn, R, Deakin, JFW and Anderson, IM (2010) Affective cognition and its disruption in mood disorders. Neuropsychopharmacology 36, 153182.CrossRefGoogle ScholarPubMed
Elliott, R, Lythe, K, Lee, R, McKie, S, Juhasz, G, Thomas, EJ, Downey, D, Deakin, J and Anderson, IM (2012) Reduced medial prefrontal responses to social interaction images in remitted depression. Archives of General Psychiatry 69, 3745.CrossRefGoogle ScholarPubMed
Everaert, J, Duyck, W and Koster, EH (2015) Emotionally biased cognitive processes: the weakest link predicts prospective changes in depressive symptom severity. PLOS ONE 10, e0124457.10.1371/journal.pone.0124457CrossRefGoogle ScholarPubMed
Fossati, P, Radtchenko, A and Boyer, P (2004) Neuroplasticity: from MRI to depressive symptoms. European Neuropsychopharmacology 14(suppl. 5), S503-S510.CrossRefGoogle ScholarPubMed
Frodl, TS, Koutsouleris, N, Bottlender, R, Born, C, Jäger, M, Scupin, I, Reiser, M, Möller, H and Meisenzahl, EM (2008) Depression-related variation in brain morphology over 3 years effects of stress? Archives of General Psychiatry 65, 11561165.CrossRefGoogle ScholarPubMed
Fu, CH, Williams, SC, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J, Andrew, CM, Pich, EM, Williams, PM and Reed, LJ (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, 877889.10.1001/archpsyc.61.9.877CrossRefGoogle ScholarPubMed
Fu, CH, Williams, SC, Brammer, MJ, Suckling, J, Kim, J, Cleare, AJ, Psych, M, Walsh, ND, Mitterschiffthaler, MT and Andrew, CM (2007) Neural responses to happy facial expressions in major depression following antidepressant treatment. The American Journal of Psychiatry 164, 599607.10.1176/ajp.2007.164.4.599CrossRefGoogle ScholarPubMed
Fu, CHY, Williams, SCR, Cleare, AJ, Scott, J, Mitterschiffthaler, MT, Walsh, ND, Donaldson, C, Suckling, J, Andrew, C, Steiner, H and Murray, RM (2008) Neural responses to sad facial expressions in major depression following cognitive behavioral therapy. Biological Psychiatry 64, 505512.CrossRefGoogle ScholarPubMed
Fu, CH, Costafreda, SG, Sankar, A, Adams, TM, Rasenick, MM, Liu, P, Donati, R, Maglanoc, LA, Horton, P and Marangell, LB (2015) Multimodal functional and structural neuroimaging investigation of major depressive disorder following treatment with duloxetine. BMC Psychiatry 15, 8292.10.1186/s12888-015-0457-2CrossRefGoogle ScholarPubMed
Goldapple, K, Segal, Z, Garson, C, Lau, M, Bieling, P, Kennedy, S and Mayberg, H (2004) Modulation of cortical-limbic pathways in major depression: treatment-specific effects of cognitive behavior therapy. Archives of General Psychiatry 61, 3441.10.1001/archpsyc.61.1.34CrossRefGoogle ScholarPubMed
Hamilton, JP and Gotlib, IH (2008) Neural substrates of increased memory sensitivity for negative stimuli in major depression. Biological Psychiatry 63, 11551162.CrossRefGoogle ScholarPubMed
Kessler, RC, Berglund, P, Demler, O, Jin, R, Merikangas, KR and Walters, EE (2005) Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry 62, 593602.CrossRefGoogle ScholarPubMed
Leppänen, JM (2006) Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Current Opinion in Psychiatry 19, 3439.CrossRefGoogle ScholarPubMed
Lyketsos, CG, Nestadt, G, Cwi, J and Heithoff, K (1994) The Life Chart Interview: a standardized method to describe the course of psychopathology. International Journal of Methods in Psychiatric Research 4, 143155.Google Scholar
Maalouf, FT, Clark, L, Tavitian, L, Sahakian, BJ, Brent, D and Phillips, ML (2012) Bias to negative emotions: a depression state-dependent marker in adolescent major depressive disorder. Psychiatry Research 198, 2833.CrossRefGoogle ScholarPubMed
MacQueen, GM, Campbell, S, McEwen, BS, Macdonald, K, Amano, S, Joffe, RT, Nahmias, C and Young, LT (2003) Course of illness, hippocampal function, and hippocampal volume in major depression. Proceedings of the National Academy of Sciences of the USA 100, 13871392.CrossRefGoogle ScholarPubMed
Mayberg, HS (1997) Limbic-cortical dysregulation: a proposed model of depression. The Journal of Neuropsychiatry and Clinical Neurosciences 9, 471481.Google ScholarPubMed
McKinnon, MC, Yucel, K, Nazarov, A and MacQueen, GM (2009) A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. Journal of Psychiatry & Neuroscience 34, 4154.Google ScholarPubMed
Neumeister, A, Drevets, WC, Belfer, I, Luckenbaugh, DA, Henry, S, Bonne, O, Herscovitch, P, Goldman, D and Charney, DS (2006) Effects of a α2C-adrenoreceptor gene polymorphism on neural responses to facial expressions in depression. Neuropsychopharmacology 31, 17501756.CrossRefGoogle Scholar
Opmeer, EM, Kortekaas, R, Tol, M, Renken, RJ, Demenescu, LR, Woudstra, S, Ter Horst, GJ, Buchem, MA, der Wee, NJ and Veltman, DJ (2015) Changes in regional brain activation related to depressive state: a 2-year longitudinal functional MRI Study. Depression and Anxiety 33, 3544.CrossRefGoogle ScholarPubMed
Penninx, BWJH, Beekman, ATF, Smit, JH, Zitman, FG, Nolen, WA, Spinhoven, P, Cuijpers, P, De Jong, PJ, Van Marwijk, HWJ and Assendelft, WJJ (2008) The Netherlands Study of Depression and Anxiety (NESDA): rationale, objectives and methods. International Journal of Methods in Psychiatric Research 17, 121140.CrossRefGoogle ScholarPubMed
Peselow, ED, Corwin, J, Fieve, RR, Rotrosen, J and Cooper, TB (1991) Disappearance of memory deficits in outpatient depressives responding to imipramine. Journal of Affective Disorders 21, 173183.CrossRefGoogle ScholarPubMed
Ramel, W, Goldin, PR, Eyler, LT, Brown, GG, Gotlib, IH and McQuaid, JR (2007) Amygdala reactivity and mood-congruent memory in individuals at risk for depressive relapse. Biological Psychiatry 61, 231239.10.1016/j.biopsych.2006.05.004CrossRefGoogle ScholarPubMed
Redlich, R, Bürger, C, Dohm, K, Grotegerd, D, Opel, N, Zaremba, D and Dannlowski, U (2017) Effects of electroconvulsive therapy on amygdala function in major depression – a longitudinal functional magnetic resonance imaging study. Psychological Medicine 47, 21662176.CrossRefGoogle ScholarPubMed
Ritchey, M, Dolcos, F, Eddington, KM, Strauman, TJ and Cabeza, R (2011) Neural correlates of emotional processing in depression: changes with cognitive behavioral therapy and predictors of treatment response. Journal of Psychiatric Research 45, 577587.CrossRefGoogle ScholarPubMed
Sapolsky, RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Archives of General Psychiatry 57, 925935.10.1001/archpsyc.57.10.925CrossRefGoogle ScholarPubMed
Schmaal, L, Veltman, DJ, van Erp, TG, Sämann, P, Frodl, T, Jahanshad, N, Loehrer, E, Tiemeier, H, Hofman, A and Niessen, W (2015) Subcortical brain alterations in major depressive disorder: findings from the ENIGMA Major Depressive Disorder working group. Molecular Psychiatry 21, 806812.CrossRefGoogle ScholarPubMed
Sheline, YI, Sanghavi, M, Mintun, MA and Gado, MH (1999) Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. The Journal of Neuroscience 19, 50345043.CrossRefGoogle Scholar
Sheline, YI, Barch, DM, Donnelly, JM, Ollinger, JM, Snyder, AZ and 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
Sternberg, DE and Jarvik, ME (1976) Memory functions in depression: Improvement with antidepressant medication. Archives of General Psychiatry 33, 219224.CrossRefGoogle Scholar
Tomioka, H, Yamagata, B, Kawasaki, S, Pu, S, Iwanami, A, Hirano, J, Nakagome, K and Mimura, M (2015) A longitudinal functional neuroimaging study in medication-naive depression after antidepressant treatment. PLoS ONE 10, e0120828.10.1371/journal.pone.0120828CrossRefGoogle ScholarPubMed
Treadway, MT, Waskom, ML, Dillon, DG, Holmes, AJ, Park, MTM, Chakravarty, MM, Dutra, SJ, Polli, FE, Iosifescu, DV, Fava, M, Gabrieli, JDE and Pizzagalli, DA (2015) Illness progression, recent stress, and morphometry of hippocampal subfields and medial prefrontal cortex in major depression. Biological Psychiatry 77, 285294.CrossRefGoogle ScholarPubMed
Tulving, E (1985) Memory and consciousness. Canadian Psychology/Psychologie Canadienne 26, 1.10.1037/h0080017CrossRefGoogle Scholar
Turk-Browne, NB, Yi, D and Chun, MM (2006) Linking implicit and explicit memory: common encoding factors and shared representations. Neuron 49, 917927.10.1016/j.neuron.2006.01.030CrossRefGoogle ScholarPubMed
Usami, M, Iwadare, Y, Kodaira, M, Watanabe, K and Saito, K (2014) Near infrared spectroscopy study of the frontopolar hemodynamic response and depressive mood in children with major depressive disorder: a pilot study. PLoS ONE 9, e86290.10.1371/journal.pone.0086290CrossRefGoogle ScholarPubMed
van Tol, MJ, van der Wee, NJA, Demenescu, LR, Nielen, MMA, Aleman, A, Renken, R, van Buchem, MA, Zitman, FG and Veltman, DJ (2011) Functional MRI correlates of visuospatial planning in out-patient depression and anxiety. Acta Psychiatrica Scandinavica 124, 273284.CrossRefGoogle ScholarPubMed
van Tol, MJ, Demenescu, LR, van der Wee, NJA, Kortekaas, R, Marjan, MAN, Boer, JD, Renken, RJ, van Buchem, MA, Zitman, FG and Aleman, A (2012) Functional magnetic resonance imaging correlates of emotional word encoding and recognition in depression and anxiety disorders. Biological Psychiatry 71, 593602.10.1016/j.biopsych.2011.11.016CrossRefGoogle ScholarPubMed
Van Wingen, GA, Van Eijndhoven, P, Cremers, HR, Tendolkar, I, Verkes, RJ, Buitelaar, JK and Fernández, G (2010) Neural state and trait bases of mood-incongruent memory formation and retrieval in first-episode major depression. Journal of Psychiatric Research 44, 527534.CrossRefGoogle ScholarPubMed
Veer, IM, Beckmann, CF, van Tol, MJ, Ferrarini, L, Milles, J, Veltman, DJ, Aleman, A, van Buchem, MA, van der Wee, NJ and Rombouts, SA (2010) Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Frontiers in Systems Neuroscience 4, 41. doi: 10.3389/fnsys.2010.00041. eCollection 2010.CrossRefGoogle ScholarPubMed
Victor, TA, Furey, ML, Fromm, SJ, Öhman, A and Drevets, WC (2010) Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Archives of General Psychiatry 67, 11281138.10.1001/archgenpsychiatry.2010.144CrossRefGoogle ScholarPubMed
Warshaw, MG, Dyck, I, Allsworth, J, Stout, RL and Keller, MB (2001) Maintaining reliability in a long-term psychiatric study: an ongoing inter-rater reliability monitoring program using the Longitudinal Interval Follow-Up Evaluation. Journal of Psychiatric Research 35, 297305.10.1016/S0022-3956(01)00030-9CrossRefGoogle Scholar
Wise, T, Cleare, AJ, Herane, A, Young, AH and Arnone, D (2014) Diagnostic and therapeutic utility of neuroimaging in depression: an overview. Neuropsychiatric Disease and Treatment 10, 15091522.Google ScholarPubMed
Young, KD, Bellgowan, PS, Bodurka, J and Drevets, WC (2015) Functional neuroimaging correlates of autobiographical memory deficits in subjects at risk for depression. Brain Sciences 5, 144164.CrossRefGoogle ScholarPubMed
Zaremba, D, Dohm, K and Redlich, R (2018) Association of brain cortical changes with relapse in patients with major depressive disorder. JAMA Psychiatry 75, 484492.CrossRefGoogle ScholarPubMed
Zimmerman, M, Posternak, MA and Chelminski, I (2004) Derivation of a definition of remission on the Montgomery-Asberg depression rating scale corresponding to the definition of remission on the Hamilton rating scale for depression. Journal of Psychiatric Research 38, 577582.10.1016/j.jpsychires.2004.03.007CrossRefGoogle ScholarPubMed
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