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

  • Hui Ai (a1) (a2), Esther M. Opmeer (a2), Jan-Bernard C. Marsman (a2), Dick J. Veltman (a3) (a4), Nic J. A. van der Wee (a5) (a6), André Aleman (a1) (a2) and Marie-José van Tol (a2)...

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.

Copyright

Corresponding author

Author for correspondence: Hui Ai, E-mail: hui.ai@hotmail.com and Marie-José van Tol, E-mail: m.j.van.tol@umcg.nl

References

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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.
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.
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.
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.
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.
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.
Bradley, BP and Mathews, A (1988) Memory bias in recovered clinical depressives. Cognition & Emotion 2, 235245.
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.
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.
Chan, SW, Goodwin, GM and Harmer, CJ (2007) Highly neurotic never-depressed students have negative biases in information processing. Psychological Medicine 37, 12811291.
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.
Disner, SG, Beevers, CG, Haigh, EAP and Beck, AT (2011) Neural mechanisms of the cognitive model of depression. Nature Reviews Neuroscience 12, 467477.
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.
Elliott, R, Zahn, R, Deakin, JFW and Anderson, IM (2010) Affective cognition and its disruption in mood disorders. Neuropsychopharmacology 36, 153182.
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.
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.
Fossati, P, Radtchenko, A and Boyer, P (2004) Neuroplasticity: from MRI to depressive symptoms. European Neuropsychopharmacology 14(suppl. 5), S503-S510.
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.
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.
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.
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.
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.
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.
Hamilton, JP and Gotlib, IH (2008) Neural substrates of increased memory sensitivity for negative stimuli in major depression. Biological Psychiatry 63, 11551162.
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.
Leppänen, JM (2006) Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Current Opinion in Psychiatry 19, 3439.
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.
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.
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.
Mayberg, HS (1997) Limbic-cortical dysregulation: a proposed model of depression. The Journal of Neuropsychiatry and Clinical Neurosciences 9, 471481.
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.
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.
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.
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.
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.
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.
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.
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.
Sapolsky, RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Archives of General Psychiatry 57, 925935.
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.
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.
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.
Sternberg, DE and Jarvik, ME (1976) Memory functions in depression: Improvement with antidepressant medication. Archives of General Psychiatry 33, 219224.
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.
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.
Tulving, E (1985) Memory and consciousness. Canadian Psychology/Psychologie Canadienne 26, 1.
Turk-Browne, NB, Yi, D and Chun, MM (2006) Linking implicit and explicit memory: common encoding factors and shared representations. Neuron 49, 917927.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.

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

  • Hui Ai (a1) (a2), Esther M. Opmeer (a2), Jan-Bernard C. Marsman (a2), Dick J. Veltman (a3) (a4), Nic J. A. van der Wee (a5) (a6), André Aleman (a1) (a2) and Marie-José van Tol (a2)...

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