Brain Imaging and Behavior

, Volume 12, Issue 1, pp 156–167 | Cite as

Imaging the up’s and down’s of emotion regulation in lifetime depression

  • Sina Radke
  • Felix Hoffstaedter
  • Leonie Löffler
  • Lydia Kogler
  • Frank Schneider
  • Jens Blechert
  • Birgit Derntl
Original Research


Reappraisal is a particularly effective strategy for influencing emotional experiences, specifically for reducing the impact of negative stimuli. Although depression has repeatedly been linked to dysfunctional behavioral and neural emotion regulation, prefrontal and amygdala engagement seems to vary with clinical characteristics and the specific regulation strategy used. Whereas previous neuroimaging research has focused on down-regulating reactions to emotionally evocative scenes, the current study compared up- and down-regulation in response to angry facial expressions in patients with depression and healthy individuals. During the initial viewing of faces, patients with depression showed hypoactivation particularly in areas implicated in emotion generation, i.e., amygdala, insula and putamen. In contrast, up-regulating negative emotions yielded stronger recruitment of core face processing areas and posterior medial frontal cortex in patients than in controls. However, group differences did not extend to resting-state functional connectivity. Recurrent depression was inversely associated with amygdala activation specifically during down-regulation, but differences in medication status may limit the current findings. Despite a pattern of reduced neural emotional reactivity in mainly medicated patients, their ‘successful’ recruitment of the regulation network for up-regulation might point toward an effective use of reappraisal when increasing negative emotions. Future studies need to address how patients might benefit from transferring this ability to adaptive goals, such as improving interpersonal emotion regulation.


Depression Emotion regulation Facial expression fMRI Reappraisal 



SR and BD were supported by JARA-BRAIN. LK, FS and BD were supported by the Deutsche Forschungsgemeinschaft (DFG; IRTG-1328). This work was supported by the Brain Imaging Facility of the Interdisciplinary Center for Clinical Research within the Faculty of Medicine at the RWTH Aachen University.

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

All authors declare no conflict of interest.

Supplementary material

11682_2017_9682_MOESM1_ESM.docx (20 kb)
Supplementary Table S1 (DOCX 19 kb)


  1. Adams, R. B., & Kleck, R. E. (2005). Effects of direct and averted gaze on the perception of facially communicated emotion. Emotion, 5(1), 3–11.CrossRefPubMedGoogle Scholar
  2. Aker, M., Harmer, C., & Landro, N. I. (2014). More rumination and less effective emotion regulation in previously depressed women with preserved executive functions. BMC Psychiatry, 14, 334. doi: 10.1186/s12888-014-0334-4.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aldao, A., Nolen-Hoeksema, S., & Schweizer, S. (2010). Emotion-regulation strategies across psychopathology: a meta-analytic review. Clinical Psychology Review, 30(2), 217–237. doi: 10.1016/j.cpr.2009.11.004.CrossRefPubMedGoogle Scholar
  4. Alloy, L. B., Abramson, L. Y., Whitehouse, W. G., Hogan, M. E., Tashman, N. A., Steinberg, D. L., et al. (1999). Depressogenic cognitive styles: predictive validity, information processing and personality characteristics, and developmental origins. Behaviour Research and Therapy, 37(6), 503–531.CrossRefPubMedGoogle Scholar
  5. Ashburner, J., & Friston, K. J. (2005). Unified segmentation. NeuroImage, 26(3), 839–851.CrossRefPubMedGoogle Scholar
  6. Beck, A. T., Rush, A. J., Shaw, B. F., & Emery, G. (1979). Cognitive therapy of depression. New York: The Guilford Press.Google Scholar
  7. Biswal, B., Yetkin, F. Z., Haughton, V. M., Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echoplanar mri. Magnetic Resonance in Medicine, 34(4), 537–541Google Scholar
  8. Blechert, J., Sheppes, G., Di Tella, C., Williams, H., & Gross, J. J. (2012). See what you think: reappraisal modulates behavioral and neural responses to social stimuli. Psychological Science, 23(4), 346–353. doi: 10.1177/0956797612438559.CrossRefPubMedGoogle Scholar
  9. Britton, J. C., Taylor, S. F., Sudheimer, K. D., & Liberzon, I. (2006). Facial expressions and complex IAPS pictures: common and differential networks. NeuroImage, 31(2), 906–919. doi: 10.1016/j.neuroimage.2005.12.050.CrossRefPubMedGoogle Scholar
  10. Buhle, J. T., Silvers, J. A., Wager, T. D., Lopez, R., Onyemekwu, C., Kober, H., et al. (2014). Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cerebral Cortex, 24(11), 2981–2990. doi: 10.1093/cercor/bht154.CrossRefPubMedGoogle Scholar
  11. Collins, D. L., Neelin, P., Peters, T. M., & Evans, A. C. (1994). Automatic 3d intersubject registration of MR volumetric data in standardized Talairach space. Journal of Computer Assisted Tomography, 18(2), 192–205.CrossRefPubMedGoogle Scholar
  12. Dillon, D. G., & Pizzagalli, D. A. (2013). Evidence of successful modulation of brain activation and subjective experience during reappraisal of negative emotion in unmedicated depression. Psychiatry Research, 212(2), 99–107. doi: 10.1016/j.pscychresns.2013.01.001.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ebner, N. C., Riediger, M., & Lindenberger, U. (2010). FACES-A database of facial expressions in young, middle-aged, and older women and men: development and validation. Behavior Research Methods, 42(1), 351–362.CrossRefPubMedGoogle Scholar
  14. Ehring, T., Fischer, S., Schnülle, J., Bösterling, A., & Tuschen-Caffier, B. (2008). Characteristics of emotion regulation in recovered depressed versus never depressed individuals. Personality and Individual Differences, 44(7), 1574–1584. doi: 10.1016/j.paid.2008.01.013.CrossRefGoogle Scholar
  15. Ehring, T., Tuschen-Caffier, B., Schnulle, J., Fischer, S., & Gross, J. J. (2010). Emotion regulation and vulnerability to depression: spontaneous versus instructed use of emotion suppression and reappraisal. Emotion, 10(4), 563–572. doi: 10.1037/a0019010.CrossRefPubMedGoogle Scholar
  16. Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage, 25(4), 1325–1335. doi: 10.1016/j.neuroimage.2004.12.034.CrossRefPubMedGoogle Scholar
  17. Erk, S., Mikschl, A., Stier, S., Ciaramidaro, A., Gapp, V., Weber, B., et al. (2010). Acute and sustained effects of cognitive emotion regulation in major depression. Journal of Neuroscience, 30(47), 15726–15734. doi: 10.1523/jneurosci.1856-10.2010.CrossRefPubMedGoogle Scholar
  18. Fales, C. L., Barch, D. M., Rundle, M. M., Mintun, M. A., Mathews, J., Snyder, A. Z., et al. (2009). Antidepressant treatment normalizes hypoactivity in dorsolateral prefrontal cortex during emotional interference processing in major depression. Journal of Affective Disorders, 112(1–3), 206–211. doi: 10.1016/j.jad.2008.04.027.CrossRefPubMedGoogle Scholar
  19. Frank, D. W., Dewitt, M., Hudgens-Haney, M., Schaeffer, D. J., Ball, B. H., Schwarz, N. F., et al. (2014). Emotion regulation: quantitative meta-analysis of functional activation and deactivation. Neuroscience and Biobehavioral Reviews, 45, 202–211. doi: 10.1016/j.neubiorev.2014.06.010.CrossRefPubMedGoogle Scholar
  20. Geva, S., Jones, P. S., Crinion, J. T., Price, C. J., Baron, J. C., & Warburton, E. A. (2011). The neural correlates of inner speech defined by voxel-based lesion-symptom mapping. Brain, 134(Pt 10), 3071–3082. doi: 10.1093/brain/awr232.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Goldapple, K., Segal, Z., Garson, C., Lau, M., Bieling, P., Kennedy, S., et al. (2004). Modulation of cortical-limbic pathways in major depression: treatment-specific effects of cognitive behavior therapy. Archives of General Psychiatry, 61(1), 34–41. doi: 10.1001/archpsyc.61.1.34.CrossRefPubMedGoogle Scholar
  22. Gotlib, I. H., & Joormann, J. (2010). Cognition and depression: current status and future directions. Annual Review of Clinical Psychology, 6, 285–312. doi: 10.1146/annurev.clinpsy.121208.131305.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Greening, S. G., Osuch, E. A., Williamson, P. C., & Mitchell, D. G. (2014). The neural correlates of regulating positive and negative emotions in medication-free major depression. Social Cognitive and Affective Neuroscience, 9(5), 628–637. doi: 10.1093/scan/nst027.CrossRefPubMedGoogle Scholar
  24. Gross, J. J. (1998). Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. Journal of Personality and Social Psychology, 74(1), 224–237.CrossRefPubMedGoogle Scholar
  25. Gross, J. J. (2015). Emotion regulation: current status and future prospects. Psychological Inquiry, 26(1), 1–26. doi: 10.1080/1047840X.2014.940781.CrossRefGoogle Scholar
  26. Gross, J. J., & John, O. P. (2003). Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. Journal of Personality and Social Psychology, 85(2), 348–362. doi: 10.1037/0022-3514.85.2.348.CrossRefPubMedGoogle Scholar
  27. Hao, L., Yang, J., Wang, Y., Zhang, S., Xie, P., Luo, Q., et al. (2015). Neural correlates of causal attribution in negative events of depressed patients: evidence from an fMRI study. Clinical Neurophysiology, 126(7), 1331–1337. doi: 10.1016/j.clinph.2014.10.146.CrossRefPubMedGoogle Scholar
  28. Hautzinger, M., Keller, F., & Kühner, C. (2006). BDI-II; Beck depressions-Inventar revision. Harcourt Test Services: Frankfurt am Main.Google Scholar
  29. Holmes, C. J., Hoge, R., Collins, L., Woods, R., Toga, A. W., & Evans, A. C. (1998). Enhancement of MR images using registration for signal averaging. Journal of Computer Assisted Tomography, 22(2), 324–333.CrossRefPubMedGoogle Scholar
  30. Kaiser, R. H., Andrews-Hanna, J. R., Wager, T. D., & Pizzagalli, D. A. (2015). Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity. JAMA Psychiatry, 72(6), 603–611. doi: 10.1001/jamapsychiatry.2015.0071.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kanske, P., Heissler, J., Schonfelder, S., & Wessa, M. (2012). Neural correlates of emotion regulation deficits in remitted depression: the influence of regulation strategy, habitual regulation use, and emotional valence. NeuroImage, 61(3), 686–693. doi: 10.1016/j.neuroimage.2012.03.089.CrossRefPubMedGoogle Scholar
  32. Kohn, N., Eickhoff, S. B., Scheller, M., Laird, A. R., Fox, P. T., & Habel, U. (2014). Neural network of cognitive emotion regulation--an ALE meta-analysis and MACM analysis. NeuroImage, 87, 345–355. doi: 10.1016/j.neuroimage.2013.11.001.CrossRefPubMedGoogle Scholar
  33. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International affective picture system (IAPS): Affective ratings of pictures and instruction manual, In Technical Report A-8. Gainesville: University of Florida.Google Scholar
  34. Morawetz, C., Bode, S., Baudewig, J., Jacobs, A. M., & Heekeren, H. R. (2015). Neural representation of emotion regulation goals. Human Brain Mapping, 37, 600–620. doi: 10.1002/hbm.23053.
  35. Morawetz, C., Kellermann, T., Kogler, L., Radke, S., Blechert, J., & Derntl, B. (2016). Intrinsic functional connectivity underlying successful emotion regulation of angry faces. Social Cognitive and Affective Neuroscience, 11(12), 1980–1991. doi: 10.1093/scan/nsw107.PubMedPubMedCentralGoogle Scholar
  36. Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., & Bandettini, P. A. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? NeuroImage, 44(3), 893–905. doi: 10.1016/j.neuroimage.2008.09.036.CrossRefPubMedGoogle Scholar
  37. Nelson, B. D., Fitzgerald, D. A., Klumpp, H., Shankman, S. A., & Phan, K. L. (2015). Prefrontal engagement by cognitive reappraisal of negative faces. Behavioural Brain Research, 279, 218–225. doi: 10.1016/j.bbr.2014.11.034.CrossRefPubMedGoogle Scholar
  38. Norbury, R., Taylor, M. J., Selvaraj, S., Murphy, S. E., Harmer, C. J., & Cowen, P. J. (2009). Short-term antidepressant treatment modulates amygdala response to happy faces. Psychopharmacology, 206(2), 197–204. doi: 10.1007/s00213-009-1597-1.CrossRefPubMedGoogle Scholar
  39. Northoff, G. (2007). Psychopathology and pathophysiology of the self in depression — neuropsychiatric hypothesis. Journal of Affective Disorders, 104(1–3), 1–14. doi: 10.1016/j.jad.2007.02.012.CrossRefPubMedGoogle Scholar
  40. Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D., et al. (2004). For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage, 23(2), 483–499. doi: 10.1016/j.neuroimage.2004.06.030.CrossRefPubMedGoogle Scholar
  41. Radke, S., Roelofs, K., & De Bruijn, E. R. A. (2013). Acting on anger: social anxiety modulates approach-avoidance tendencies after oxytocin administration. Psychological Science, 24(8), 1573–1578.CrossRefPubMedGoogle Scholar
  42. Reitan, R. (1956). Trail making test: Manual for administration, scoring and interpretation. Indianapolis: Indiana University Press.Google Scholar
  43. Rive, M. M., Mocking, R. J., Koeter, M. W., van Wingen, G., de Wit, S. J., van den Heuvel, O. A., et al. (2015). State-dependent differences in emotion regulation between unmedicated bipolar disorder and major depressive disorder. JAMA Psychiatry, 72(7), 687–696. doi: 10.1001/jamapsychiatry.2015.0161.CrossRefPubMedGoogle Scholar
  44. Saad, Z. S., Gotts, S. J., Murphy, K., Chen, G., Jo, H. J., Martin, A., et al. (2012). Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connectivity, 2(1), 25–32. doi: 10.1089/brain.2012.0080.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Satterthwaite, T. D., Elliott, M. A., Gerraty, R. T., Ruparel, K., Loughead, J., Calkins, M. E., et al. (2013). An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. NeuroImage, 64, 240–256. doi: 10.1016/j.neuroimage.2012.08.052.CrossRefPubMedGoogle Scholar
  46. Schilbach, L., Muller, V. I., Hoffstaedter, F., Clos, M., Goya-Maldonado, R., Gruber, O., et al. (2014). Meta-analytically informed network analysis of resting state FMRI reveals hyperconnectivity in an introspective socio-affective network in depression. PloS One, 9(4), e94973. doi: 10.1371/journal.pone.0094973.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Schmidt, K.-H., & Metzler, P. (1992). Wortschatztest (WST). Beltz Test GmbH: Weinheim.Google Scholar
  48. Smoski, M. J., Keng, S. L., Schiller, C. E., Minkel, J., & Dichter, G. S. (2013). Neural mechanisms of cognitive reappraisal in remitted major depressive disorder. Journal of Affective Disorders, 151(1), 171–177. doi: 10.1016/j.jad.2013.05.073.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Smoski, M. J., Keng, S. L., Ji, J. L., Moore, T., Minkel, J., & Dichter, G. S. (2015). Neural indicators of emotion regulation via acceptance vs reappraisal in remitted major depressive disorder. Social Cognitive and Affective Neuroscience, 10(9), 1187–1194. doi: 10.1093/scan/nsv003.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., & Jacobs, G. A. (1983). Manual for the state-trait anxiety inventory. Palo Alto: Consulting Psychologists Press.Google Scholar
  51. Stuhrmann, A., Suslow, T., & Dannlowski, U. (2011). Facial emotion processing in major depression: a systematic review of neuroimaging findings. Biol Mood Anxiety Disord, 1(10), 1–17.Google Scholar
  52. Von Aster, M., Neubauer, A., & Horn, R. (2006). Hamburg-Wechsler-Intelligenz-Test für Erwachsene III. Frankfurt: Harcourt.Google Scholar
  53. Wittchen, H. U., Wunderlich, U., Gruschwitz, S., & Zaudig, M. (1997). SKID-I. Strukturiertes Klinisches Interview für DSM-IV. Achse I: Psychische Störungen. Interviewheft. Göttingen: Hogrefe.Google Scholar
  54. Ziv, M., Goldin, P. R., Jazaieri, H., Hahn, K. S., & Gross, J. J. (2013). Emotion regulation in social anxiety disorder: behavioral and neural responses to three socio-emotional tasks. Biol Mood Anxiety Disord, 3(1), 20. doi: 10.1186/2045-5380-3-20.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of Psychiatry, Psychotherapy and Psychosomatics, Medical FacultyRWTH Aachen UniversityAachenGermany
  2. 2.Jülich Aachen Research Alliance (JARA) - BRAIN Institute Brain Structure-Function Relationships: Decoding the Human Brain at systemic levelsForschungszentrum Jülich GmbH and RWTH Aachen UniversityJülichGermany
  3. 3.Institute of Neuroscience and Medicine (INM-1)Research Centre JülichJülichGermany
  4. 4.Institute of Clinical Neuroscience and Medical PsychologyHeinrich Heine University DüsseldorfDüsseldorfGermany
  5. 5.Department of Psychiatry and Psychotherapy, Medical SchoolUniversity of TübingenTübingenGermany
  6. 6.Department of PsychologyUniversity of SalzburgSalzburgAustria
  7. 7.Centre for Cognitive NeuroscienceUniversity of SalzburgSalzburgAustria
  8. 8.Werner Reichardt Center for Integrative NeuroscienceUniversity of TübingenTübingenGermany
  9. 9.LEAD Graduate SchoolUniversity of TübingenTübingenGermany

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