Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T13:09:56.490Z Has data issue: false hasContentIssue false

Interaction between a history of depression and rumination on neural response to emotional faces

Published online by Cambridge University Press:  09 February 2011

E. J. Thomas*
Affiliation:
Neuroscience and Psychiatry Unit, University of Manchester and Manchester Academic Health Science Centre, UK
R. Elliott
Affiliation:
Neuroscience and Psychiatry Unit, University of Manchester and Manchester Academic Health Science Centre, UK
S. McKie
Affiliation:
Neuroscience and Psychiatry Unit, University of Manchester and Manchester Academic Health Science Centre, UK
D. Arnone
Affiliation:
Neuroscience and Psychiatry Unit, University of Manchester and Manchester Academic Health Science Centre, UK
D. Downey
Affiliation:
Imaging Science and Biomedical Engineering Department, University of Manchester and Manchester Academic Health Science Centre, UK
G. Juhasz
Affiliation:
Neuroscience and Psychiatry Unit, University of Manchester and Manchester Academic Health Science Centre, UK
J. F. W. Deakin
Affiliation:
Neuroscience and Psychiatry Unit, University of Manchester and Manchester Academic Health Science Centre, UK
I. M. Anderson
Affiliation:
Neuroscience and Psychiatry Unit, University of Manchester and Manchester Academic Health Science Centre, UK
*
*Address for correspondence: Dr E. J. Thomas, Neuroscience and Psychiatry Unit, G.704 Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK. (Email: [email protected])

Abstract

Background

Both past depressive episodes and the personality trait of depressive rumination are strong risk factors for future depression. Depression is associated with abnormal emotional processing, which may be a neurobiological marker for vulnerability to depression. A consistent picture has yet to emerge as to how a history of depression and the tendency to ruminate influence emotional processing. The aim of this study was to investigate the relationship between rumination, past depression and neural responses when processing face emotions.

Method

The Ruminative Responses Scale (RRS) was completed by 30 remitted depressives and 37 controls who underwent functional magnetic resonance imaging (fMRI) scanning while viewing happy, sad, fearful and neutral faces.

Results

The remitted depressives showed overall reductions in neural responses to negative emotions relative to the controls. However, in the remitted depressives, but not the controls, RRS scores were correlated with increased neural responses to negative emotions and decreased responses to happiness in limbic regions.

Conclusions

Automatic emotion processing biases and rumination seem to be correlated to aspects of vulnerability to depression. However, remission from depression may be maintained by a general suppression of limbic responsiveness to negative emotion.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolphs, R, Tranel, D, Damasio, H, Damasio, A (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669672.CrossRefGoogle Scholar
Almeida, JRC, Versace, A, Hassel, S, Kupfer, DJ, Phillips, ML (2010). Elevated amygdala activity to sad facial expressions: a state marker of bipolar but not unipolar depression. Biological Psychiatry 67, 414421.CrossRefGoogle Scholar
Anderson, IM, Del-Ben, CM, McKie, S, Richardson, P, Williams, SR, Elliott, R, Deakin, JFW (2007). Citalopram modulation of neuronal responses to face emotion: an fMRI study. Neuroreport 18, 13511355.CrossRefGoogle Scholar
Bhagwagar, Z, Cowen, PJ (2008). ‘It's not over when it's over’: persistent neurobiological abnormalities in recovered depressed patients. Psychological Medicine 38, 307313.CrossRefGoogle Scholar
Bhagwagar, Z, Cowen, PJ, Goodwin, GM, Harmer, CJ (2004). Normalization of enhanced fear recognition by acute SSRI treatment in subjects with a previous history of depression. American Journal of Psychiatry 161, 166168.CrossRefGoogle ScholarPubMed
Bouhuys, AL, Geerts, E, Gordijn, MCM (1999). Depressed patients' perceptions of facial emotions in depressed and remitted states are associated with relapse: a longitudinal study. Journal of Nervous and Mental Disease 187, 595602.CrossRefGoogle ScholarPubMed
Bradley, BP, Mogg, K, Millar, N, Bonham Carter, C, Fergusson, E, Jenkins, J, Parr, M (1997). Attentional biases for emotional faces. Cognition and Emotion 11, 2542.CrossRefGoogle Scholar
Breiter, HC, Etcoff, NL, Whalen, PJ, Kennedy, WA, Rauch, SL, Buckner, RL, Strauss, MM, Hyman, SE, Rosen, BR (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17, 875887.CrossRefGoogle ScholarPubMed
Canli, T (2008). Toward a neurogenetic theory of neuroticism. Molecular and Biophysical Mechanisms of Arousal, Alertness, and Attention 1129, 153174.Google Scholar
Canli, T, Sivers, H, Whitfield, SL, Gotlib, IH, Gabrieli, JDE (2002). Amygdala response to happy faces as a function of extraversion. Science 296, 2191.CrossRefGoogle ScholarPubMed
Canli, T, Zhao, Z, Desmond, JE, Kang, EJ, Gross, J, Gabrieli, JDE (2001). An fMRI study of personality influences on brain reactivity to emotional stimuli. Behavioral Neuroscience 115, 3342.CrossRefGoogle ScholarPubMed
Chan, SWY, Goodwin, GM, Harmer, CJ (2007). Highly neurotic never-depressed students have negative biases in information processing. Psychological Medicine 37, 12811291.CrossRefGoogle ScholarPubMed
Chan, SWY, Norbury, R, Goodwin, GM, Harmer, CJ (2009). Risk for depression and neural responses to fearful facial expressions of emotion. British Journal of Psychiatry 194, 139145.CrossRefGoogle ScholarPubMed
Dannlowski, U, Ohrmann, P, Bauer, J, Deckert, J, Hohoff, C, Kugel, H, Arolt, V, Heindel, W, Kersting, A, Baune, BT, Suslow, T (2008). 5-HTTLPR biases amygdala activity in response to masked facial expressions in major depression. Neuropsychopharmacology 33, 418424.CrossRefGoogle ScholarPubMed
Deakin, JFW (1991). Depression and 5HT. International Clinical Psychopharmacology 6, 2331.CrossRefGoogle ScholarPubMed
Deakin, JFW (1993). A review of clinical efficacy of 5-HT(1A) agonists in anxiety and depression. Journal of Psychopharmacology 7, 283289.CrossRefGoogle Scholar
Del-Ben, C, Deakin, JFW, McKie, S, Delvai, N, Williams, S, Elliott, R, Dolan, M, Anderson, IM (2005). The effect of citalopram pretreatment on neuronal responses to neuropsychological tasks in normal volunteers: an fMRI study. Neuropsychopharmacology 30, 17241734.CrossRefGoogle ScholarPubMed
Drevets, WC, Frank, E, Price, JC, Kupfer, DJ, Holt, D, Greer, PJ, Huang, YY, Gautier, C, Mathis, C (1999). PET imaging of serotonin 1A receptor binding in depression. Biological Psychiatry 46, 13751387.CrossRefGoogle ScholarPubMed
Ekman, P, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version (SCID-I). Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Fitzgerald, DA, Angstadt, M, Jelsone, LM, Nathan, PJ, Phan, KL (2006). Beyond threat: amygdala reactivity across multiple expressions of facial affect. NeuroImage 30, 14411448.CrossRefGoogle ScholarPubMed
Fu, CHY, Mourao-Miranda, J, Costafreda, SG, Khanna, A, Marquand, AF, Williams, SC, Brammer, MJ (2008). Pattern classification of sad facial processing: toward the development of neurobiological markers in depression. Biological Psychiatry 63, 656662.CrossRefGoogle ScholarPubMed
Fu, CHY, Williams, SCR, Brammer, MJ, Suckling, J, Kim, J, Cleare, AJ, Walsh, ND, Mitterschiffthaler, MT, Andrew, CM, Pich, EM, Bullmore, ET (2007). Neural responses to happy facial expressions in major depression following antidepressant treatment. American Journal of Psychiatry 164, 599607.CrossRefGoogle ScholarPubMed
Fu, CHY, Williams, SCR, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J, Andrew, CM, 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
Gotlib, IH, Sivers, H, Gabrieli, JDE, Whitfield-Gabrieli, S, Goldin, P, Minor, KL, Canli, T (2005). Subgenual anterior cingulate activation to valenced emotional stimuli in major depression. Neuroreport 16, 17311734.CrossRefGoogle ScholarPubMed
Graeff, FG, Guimaraes, FS, DeAndrade, TGCS, Deakin, JFW (1996). Role of 5-HT in stress, anxiety, and depression. Pharmacology, Biochemistry and Behavior 54, 129141.CrossRefGoogle ScholarPubMed
Gur, RC, Erwin, RJ, Gur, RE, Zwil, AS, Heimberg, C, Kraemer, HC (1992). Facial emotion discrimination. 2. Behavioral findings in depression. Psychiatry Research 42, 241251.CrossRefGoogle ScholarPubMed
Haas, BW, Constable, RT, Canli, T (2008). Stop the sadness: neuroticism is associated with sustained medial prefrontal cortex response to emotional facial expressions. NeuroImage 42, 385392.CrossRefGoogle ScholarPubMed
Haas, BW, Omura, K, Constable, RT, Canli, T (2007). Emotional conflict and neuroticism: personality-dependent activation in the amygdala and subgenual anterior cingulate. Behavioral Neuroscience 121, 249256.CrossRefGoogle ScholarPubMed
Hamilton, M (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology 32, 5055.CrossRefGoogle ScholarPubMed
Harmer, CJ, O'Sullivan, , Favaron, E, Massey-Chase, R, Ayres, R, Reinecke, A, Goodwin, GM, Cowen, PJ (2009). Effect of acute antidepressant administration on negative affective bias in depressed patients. American Journal of Psychiatry 166, 11781184.CrossRefGoogle ScholarPubMed
Joormann, J (2006). Differential effects of rumination and dysphoria on the inhibition of irrelevant emotional material: evidence from a negative priming task. Cognitive Therapy and Research 30, 149160.CrossRefGoogle Scholar
Joormann, J, Dkane, M, Gotlib, IH (2006). Adaptive and maladaptive components of rumination? Diagnostic specificity and relation to depressive biases. Behavior Therapy 37, 269280.CrossRefGoogle ScholarPubMed
Joormann, J, Gotlib, IH (2006). Is this happiness I see? Biases in the identification of emotional facial expressions in depression and social phobia. Journal of Abnormal Psychology 115, 705714.CrossRefGoogle ScholarPubMed
Joormann, J, Gotlib, IH (2007). Selective attention to emotional faces following recovery from depression. Journal of Abnormal Psychology 116, 8085.CrossRefGoogle ScholarPubMed
Just, N, Alloy, LB (1997). The response styles theory of depression: tests and an extension of the theory. Journal of Abnormal Psychology 106, 221229.CrossRefGoogle Scholar
Keedwell, PA, Andrew, C, Williams, SCR, Brammer, MJ, Phillips, ML (2005). A double dissociation of ventromedial prefrontal cortical responses to sad and happy stimuli in depressed and healthy individuals. Biological Psychiatry 58, 495503.CrossRefGoogle ScholarPubMed
Kendler, KS, Gatz, M, Gardner, CO, Pedersen, NL (2006). Personality and major depression: a Swedish longitudinal, population-based twin study. Archives of General Psychiatry 63, 11131120.CrossRefGoogle ScholarPubMed
Lawrence, NS, Williams, AM, Surguladze, S, Giampietro, V, Brammer, MJ, Andrew, C, Frangou, S, Ecker, C, Phillips, ML (2004). Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biological Psychiatry 55, 578587.CrossRefGoogle ScholarPubMed
Lee, BT, Seok, JH, Lee, BC, Cho, SW, Yoon, BJ, Lee, KU, Chae, JH, Choi, IG, Ham, BJ (2008). Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 32, 778785.CrossRefGoogle ScholarPubMed
Liotti, M, Mayberg, HS, McGinnis, S, Brannan, SL, Jerabek, P (2002). Unmasking disease-specific cerebral blood flow abnormalities: mood challenge in patients with remitted unipolar depression. American Journal of Psychiatry 159, 18301840.CrossRefGoogle ScholarPubMed
Maldjian, JA, Laurienti, PJ, Burdette, JH (2004). Precentral gyrus discrepancy in electronic versions of the Talairach atlas. NeuroImage 21, 450455.CrossRefGoogle ScholarPubMed
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 12331239.CrossRefGoogle ScholarPubMed
Mayberg, HS, Brannan, SK, Tekell, JL, Silva, JA, Mahurin, RK, McGinnis, S, Jerabek, PA (2000). Regional metabolic effects of fluoxetine in major depression: serial changes and relationship to clinical response. Biological Psychiatry 48, 830843.CrossRefGoogle ScholarPubMed
Mayberg, HS, Liotti, M, Brannan, SK, McGinnis, S, Mahurin, RK, Jerabek, PA, Silva, JA, Tekell, JL, Martin, CC, Lancaster, JL, Fox, PT (1999). Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. American Journal of Psychiatry 156, 675682.CrossRefGoogle ScholarPubMed
McCrae, RR, John, OP (1992). An introduction to the 5-factor model and its applications. Journal of Personality 60, 175215.CrossRefGoogle Scholar
Miranda, R, Nolen-Hoeksema, S (2007). Brooding and reflection: rumination predicts suicidal ideation at 1-year follow-up in a community sample. Behaviour Research and Therapy 45, 30883095.CrossRefGoogle Scholar
Monk, CS, Klein, RG, Telzer, EH, Schroth, EA, Mannuzza, S, Moulton, JL, Guardino, M, Masten, CL, Clure-Tone, EB, Fromm, S, Blair, RJ, Pine, DS, Ernst, M (2008). Amygdala and nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression. American Journal of Psychiatry 165, 9098.CrossRefGoogle ScholarPubMed
Montgomery, SA, Asberg, M (1979). New depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382389.CrossRefGoogle ScholarPubMed
Morris, JS, Frith, CD, Perrett, DI, Rowland, D, Young, AW, Calder, AJ, Dolan, RJ (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812815.CrossRefGoogle ScholarPubMed
Neumeister, A, Drevets, WC, Belfer, I, Luckenbaugh, DA, Henry, S, Bonne, O, Herscovitchs, P, Goldman, D, Charney, DS (2006). Effects of alpha(2C)-adrenoreceptor gene polymorphism on neural responses to facial expressions in depression. Neuropsychopharmacology 31, 17501756.CrossRefGoogle ScholarPubMed
Nolen-Hoeksema, S (1991). Responses to depression and their effects on the duration of depressive episodes. Journal of Abnormal Psychology 100, 569582.CrossRefGoogle ScholarPubMed
Nolen-Hoeksema, S, Morrow, J (1991). A prospective-study of depression and posttraumatic stress symptoms after a natural disaster: the 1989 Loma Prieta Earthquake. Journal of Personality and Social Psychology 61, 115121.CrossRefGoogle ScholarPubMed
Norbury, R, Selvaraj, S, Taylor, MJ, Harmer, C, Cowen, PJ (2010). Increased neural response to fear in patients recovered from depression: a 3T functional magnetic resonance imaging study. Psychological Medicine 40, 425432.CrossRefGoogle ScholarPubMed
Persad, SM, Polivy, J (1993). Differences between depressed and nondepressed individuals in the recognition of and response to facial emotional cues. Journal of Abnormal Psychology 102, 358368.CrossRefGoogle ScholarPubMed
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16, 331348.CrossRefGoogle ScholarPubMed
Raes, F, Hermans, D, Williams, JMG (2006). Negative bias in the perception of others' facial emotional expressions in major depression: the role of depressive rumination. Journal of Nervous and Mental Disease 194, 796799.CrossRefGoogle ScholarPubMed
Ray, RD, Ochsner, KN, Cooper, JC, Robertson, ER, Gabrieli, JDE, Gross, JJ (2005). Individual differences in trait rumination and the neural systems supporting cognitive reappraisal. Cognitive Affective and Behavioral Neuroscience 5, 156168.CrossRefGoogle ScholarPubMed
Roberts, JE, Gilboa, E, Gotlib, IH (1998). Ruminative response style and vulnerability to episodes of dysphoria: gender, neuroticism, and episode duration. Cognitive Therapy and Research 22, 401423.CrossRefGoogle Scholar
Roelofs, J, Huibers, M, Peeters, F, Arntz, A, van Os, J (2008). Rumination and worrying as possible mediators in the relation between neuroticism and symptoms of depression and anxiety in clinically depressed individuals. Behaviour Research and Therapy 46, 12831289.CrossRefGoogle ScholarPubMed
Sander, D, Grafman, J, Zalla, T (2003). The human amygdala: an evolved system for relevance detection. Reviews in the Neurosciences 14, 303316.CrossRefGoogle ScholarPubMed
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, Steinhauer, SR, Thase, ME, Stenger, VA, Carter, CS (2002). Can't shake that feeling: assessment of sustained event-related fMRI amygdala activity in response to emotional information in depressed individuals. Biological Psychiatry 51, 693707.CrossRefGoogle ScholarPubMed
Spasojevic, J, Alloy, LB (2001). Rumination as a common mechanism relating depressive risk factors to depression. Emotion 1, 2537.CrossRefGoogle ScholarPubMed
Surguladze, S, Brammer, MJ, Keedwell, P, Giampietro, V, Young, AW, Travis, MJ, Williams, SCR, Phillips, ML (2005). A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biological Psychiatry 57, 201209.CrossRefGoogle ScholarPubMed
Surguladze, SA, Young, AW, Senior, C, Brebion, G, Travis, MJ, Phillips, ML (2004). Recognition accuracy and response bias to happy and sad facial expressions in patients with major depression. Neuropsychology 18, 212218.CrossRefGoogle ScholarPubMed
Suslow, T, Junghanns, K, Arolt, V (2001). Detection of facial expressions of emotions in depression. Perceptual and Motor Skills 92, 857868.CrossRefGoogle ScholarPubMed
Treynor, W, Gonzalez, R, Nolen-Hoeksema, S (2003). Rumination reconsidered: a psychometric analysis. Cognitive Therapy and Research 27, 247259.CrossRefGoogle Scholar
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