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Subgenual activation and the finger of blame: individual differences and depression vulnerability

Published online by Cambridge University Press:  25 September 2020

Karen E Lythe ,
Jennifer A Gethin ,
Clifford I Workman ,
Matthew A. Lambon Ralph ,
John F.W. Deakin ,
Jorge Moll  and
Roland Zahn Open the ORCID record for Roland Zahn [Opens in a new window]
Karen E Lythe
Affiliation:
The University of Manchester & Manchester Academic Health Sciences Centre, School of Psychological Sciences, Neuroscience and Aphasia Research Unit, Manchester, M13 9PL, UK
Jennifer A Gethin
Affiliation:
The University of Manchester & Manchester Academic Health Sciences Centre, School of Psychological Sciences, Neuroscience and Aphasia Research Unit, Manchester, M13 9PL, UK
Clifford I Workman
Affiliation:
The University of Manchester & Manchester Academic Health Sciences Centre, School of Psychological Sciences, Neuroscience and Aphasia Research Unit, Manchester, M13 9PL, UK The University of Manchester & Manchester Academic Health Sciences Centre, Institute of Brain, Behaviour and Mental Health, Neuroscience & Psychiatry Unit, Manchester, M13 9PL, UK
Matthew A. Lambon Ralph
Affiliation:
The University of Manchester & Manchester Academic Health Sciences Centre, School of Psychological Sciences, Neuroscience and Aphasia Research Unit, Manchester, M13 9PL, UK MRC Cognition and Brain Sciences Unit, University of Cambridge, 15 Chaucer Road, Cambridge, CB2 7EF, UK
John F.W. Deakin
Affiliation:
The University of Manchester & Manchester Academic Health Sciences Centre, Institute of Brain, Behaviour and Mental Health, Neuroscience & Psychiatry Unit, Manchester, M13 9PL, UK
Jorge Moll
Affiliation:
Cognitive and Behavioral Neuroscience Unit, D'Or Institute for Research and Education (IDOR), 22280-080 - Rio de Janeiro, RJ, Brazil
Roland Zahn*
Affiliation:
The University of Manchester & Manchester Academic Health Sciences Centre, School of Psychological Sciences, Neuroscience and Aphasia Research Unit, Manchester, M13 9PL, UK Cognitive and Behavioral Neuroscience Unit, D'Or Institute for Research and Education (IDOR), 22280-080 - Rio de Janeiro, RJ, Brazil Institute of Psychiatry, Psychology & Neuroscience, Department of Psychological Medicine, Centre for Affective Disorders, King's College London, London, SE5 8AZ, UK National Service for Affective Disorders, South London and Maudsley NHS Foundation Trust, London, SE5 8AZ, UK
*
Author for correspondence: Roland Zahn, E-mail: [email protected]
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Abstract

Background

Subgenual cingulate cortex (SCC) responses to self-blaming emotion-evoking stimuli were previously found in individuals prone to self-blame with and without a history of major depressive disorder (MDD). This suggested SCC activation reflects self-blaming emotions such as guilt, which are central to models of MDD vulnerability.

Method

Here, we re-examined these hypotheses in an independent larger sample. A total of 109 medication-free participants (70 with remitted MDD and 39 healthy controls) underwent fMRI whilst judging self- and other-blaming emotion-evoking statements. They also completed validated questionnaires of proneness to self-blaming emotions including those related to internal (autonomy) and external (sociotropy) evaluation, which were subjected to factor analysis.

Results

An interaction between group (remitted MDD v. Control) and condition (self- v. other-blame) was observed in the right SCC (BA24). This was due to higher SCC signal for self-blame in remitted MDD and higher other-blame-selective activation in Control participants. Across the whole sample, extracted SCC activation cluster averages for self- v. other-blame were predicted by a regression model which included the reliable components derived from our factor analysis of measures of proneness to self-blaming emotions. Interestingly, this prediction was solely driven by autonomy/self-criticism, and adaptive guilt factors, with no effect of sociotropy/dependency.

Conclusions

Despite confirming the prediction of SCC activation in self-blame-prone individuals and those vulnerable to MDD, our results suggest that SCC activation reflects blame irrespective of where it is directed rather than selective for self. We speculate that self-critical individuals have more extended SCC representations for blame in the context of self-agency.

Keywords

Attachment styledepressionemotionsfMRIfrontal cortexindividual differences
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 8 , June 2022 , pp. 1560 - 1568
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Abramson, L. Y., Seligman, M. E. P., & Teasdale, J. D. (1978). Learned helplessness in humans - critique and reformulation. Journal of Abnormal Psychology, 87(1), 49–74.CrossRefGoogle ScholarPubMed
Andersson, J. L. R., Hutton, C., Ashburner, J., Turner, R., & Friston, K. (2001). Modeling geometric deformations in EPI time series. Neuroimage, 13(5), 903–919. doi:10.1006/nimg.2001.0746.CrossRefGoogle ScholarPubMed
Balint, M. (1959). Thrills and regressions. London: Maresfield Library.Google Scholar
Basile, B., Mancini, F., Macaluso, E., Caltagirone, C., Frackowiak, R. S., & Bozzali, M. (2011). Deontological and altruistic guilt: Evidence for distinct neurobiological substrates. Human Brain Mapping, 32(2), 229–239.CrossRefGoogle ScholarPubMed
Beck, A. T., Rush, A. J., Shaw, B. F., & Emery, G. (1979). Cognitive therapy of depression. New York: Guilford Press.Google Scholar
Beck, A. T., Steer, R. A., & Carbin, M. G. (1988). Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clinical Psychology Review, 8(1), 77–100.CrossRefGoogle Scholar
Bowlby, J. (1977). The making and breaking of affectional bonds. I. Aetiology and psychopathology in the light of attachment theory. An expanded version of the Fiftieth Maudsley Lecture, delivered before the Royal College of Psychiatrists, 19 November 1976. British Journal of Psychiatry, 130, 201–210.CrossRefGoogle Scholar
Brett, M., Anton, J.-L., Valabregue, R., & Poline, J.-B. (2002). Region of interest analysis using an SPM toolbox. Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.Google Scholar
Clark, D. A., & Beck, A. T. (1991). Personality-Factors in dysphoria - a psychometric refinement of Beck Sociotropy-Autonomy Scale. Journal of Psychopathology and Behavioral Assessment, 13(4), 369–388. doi:10.1007/Bf00960448.CrossRefGoogle Scholar
Clark, D. A., Steer, R. A., Beck, A. T., & Ross, L. (1995). Psychometric characteristics of revised sociotropy and autonomy scales in college students. Behaviour Research and Therapy, 33(3), 325–334.CrossRefGoogle ScholarPubMed
Clark, L. A., Watson, D., & Mineka, S. (1994). Temperament, personality, and the mood and anxiety disorders. Journal of Abnormal Psychology, 103(1), 103–116. doi:10.1037/0021-843x.103.1.103.CrossRefGoogle ScholarPubMed
Decety, J., Skelly, L. R., & Kiehl, K. A. (2013). Brain response to empathy-eliciting scenarios involving pain in incarcerated individuals with psychopathy. JAMA Psychiatry, 70(6), 638–645. doi:10.1001/jamapsychiatry.2013.27.CrossRefGoogle ScholarPubMed
Drevets, W. C. (1998). Functional neuroimaging studies of depression: The anatomy of melancholia. Annual Review of Medicine, 49, 341– + . doi:10.1146/annurev.med.49.1.341.CrossRefGoogle ScholarPubMed
Drevets, W. C., Ongur, D., & Price, J. L. (1998). Neuroimaging abnormalities in the subgenual prefrontal cortex: Implications for the pathophysiology of familial mood disorders. Molecular Psychiatry, 3(3), 220–226. doi:10.1038/sj.mp.4000370.CrossRefGoogle ScholarPubMed
Eaton, W. W., Shao, H., Nestadt, G., Lee, H. B., Bienvenu, O. J., & Zandi, P. (2008). Population-based study of first onset and chronicity in major depressive disorder. Archives of General Psychiatry, 65(5), 513–520.CrossRefGoogle ScholarPubMed
Ebert, D., & Ebmeier, K. P. (1996). The role of the cingulate gyrus in depression: From functional anatomy to neurochemistry. Biological Psychiatry, 39(12), 1044–1050.CrossRefGoogle ScholarPubMed
Fehse, K., Silveira, S., Elvers, K., & Blautzik, J. (2015). Compassion, guilt and innocence: An fMRI study of responses to victims who are responsible for their fate. Social Neuroscience, 10(3), 243–252. doi:10.1080/17470919.2014.980587.CrossRefGoogle ScholarPubMed
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2002). Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition. (SCID-I/P). New York, NY: Biometrics Research, New York State Psychiatric Institute.Google Scholar
Freud, S. (1917). Trauer und melancholie. Zeitschrift fuer Aerztliche Psychoanalyse, 4(6), 288–301.Google Scholar
Green, S., Lambon Ralph, M. A., Moll, J., Deakin, J. F. W., & Zahn, R. (2012). Guilt-Selective functional disconnection of anterior temporal and subgenual cortices in Major depressive disorder. Archives of General Psychiatry, 69(10), 1014–1021.CrossRefGoogle ScholarPubMed
Green, S., Lambon Ralph, M. A., Moll, J., Zakrzewski, J., Deakin, J. F., Grafman, J., … Zahn, R. (2013). The neural basis of conceptual-emotional integration and its role in major depressive disorder. Social Neuroscience, 8(5), 417–433.CrossRefGoogle ScholarPubMed
Green, S., Moll, J., Deakin, J. F., Hulleman, J., & Zahn, R. (2013a). Proneness to decreased negative emotions in major depressive disorder when blaming others rather than oneself. Psychopathology, 46(1), 34–44. doi:10.1159/000338632.CrossRefGoogle Scholar
Green, S., Ralph, M. A. L., Moll, J., Stamatakis, E. A., Grafman, J., & Zahn, R. (2010). Selective functional integration between anterior temporal and distinct fronto-mesolimbic regions during guilt and indignation. Neuroimage, 52(4), 1720–1726.CrossRefGoogle ScholarPubMed
Hamani, C., Mayberg, H., Stone, S., Laxton, A., Haber, S., & Lozano, A. M. (2011). The subcallosal cingulate gyrus in the context of Major depression. Biological Psychiatry, 69(4), 301–308. doi:10.1016/j.biopsych.2010.09.034.CrossRefGoogle ScholarPubMed
Hare, R. D. (2003). The hare psychopathy checklist-revised (2nd ed.). Toronto: Multi-Health Systems.Google Scholar
Harenski, C. L., & Hamann, S. (2006). Neural correlates of regulating negative emotions related to moral violations. Neuroimage, 30(1), 313–324.CrossRefGoogle ScholarPubMed
Higgins, E. T. (1987). Self-discrepancy - a theory relating self and affect. Psychological Review, 94(3), 319–340.CrossRefGoogle ScholarPubMed
Immordino-Yang, M. H., McColl, A., Damasio, H., & Damasio, A. (2009). Neural correlates of admiration and compassion. Proceedings of the National Academy of Sciences of the United States of America, 106(19), 8021–8026. doi:10.1073/pnas.0810363106.CrossRefGoogle ScholarPubMed
Janoff-Bulman, R. (1979). Characterological versus behavioral self-blame: Inquiries into depression and rape. Journal of Personality and Social Psychology, 37(10), 1798.CrossRefGoogle ScholarPubMed
Judas, M., Cepanec, M., & Sedmak, G. (2012). Brodmann's map of the human cerebral Cortex - or Brodmann's maps? Translational Neuroscience, 3(1), 67–74. doi:10.2478/s13380-012-0009-x.CrossRefGoogle Scholar
Kédia, G., Berthoz, S., Wessa, M., Hilton, D., & Martinot, J.-L. (2008). An agent harms a victim: A functional magnetic resonance imaging study on specific moral emotions. Journal of Cognitive Neuroscience, 20(10), 1788–1798.CrossRefGoogle Scholar
Krueger, F., McCabe, K., Moll, J., Kriegeskorte, N., Zahn, R., Strenziok, M., … Grafman, J. (2007). Neural correlates of trust. Proceedings of the National Academy of Sciences of the United States of America, 104(50), 20084–20089.CrossRefGoogle ScholarPubMed
Leckman, J. F., Caruso, K. A., Prusoff, B. A., Weissman, M. M., Merikangas, K. R., & Pauls, D. L. (1984). Appetite disturbance and excessive guilt in major depression - use of family study data to define depressive subtypes. Archives of General Psychiatry, 41(9), 839–844.CrossRefGoogle ScholarPubMed
Lockwood, P. L., & Wittmann, M. K. (2018). Ventral anterior cingulate cortex and social decision-making. Neuroscience and Biobehavioral Reviews, 92, 187–191. doi:10.1016/j.neubiorev.2018.05.030.CrossRefGoogle ScholarPubMed
Lythe, K. E., Moll, J., Gethin, J. A., Workman, C., Green, S., Lambon Ralph, M. A., … Zahn, R. (2015). Self-blame-selective hyperconnectivity between anterior temporal and subgenual cortices and prediction of recurrent depressive episodes. JAMA Psychiatry, 72(11), 1–8.CrossRefGoogle ScholarPubMed
Marchesotti, S., Martuzzi, R., Schurger, A., Blefari, M. L., del Millán, J. R., Bleuler, H., & Blanke, O. (2017). Cortical and subcortical mechanisms of brain-machine interfaces. Human Brain Mapping, 38(6), 2971–2989. doi:10.1002/hbm.23566.CrossRefGoogle ScholarPubMed
Mayberg, H. S., Lozano, A. M., Voon, V., McNeely, H. E., Seminowicz, D., Hamani, C., … Kennedy, S. H. (2005). Deep brain stimulation for treatment-resistant depression. Neuron, 45(5), 651–660. doi:10.1016/j.neuron.2005.02.014.CrossRefGoogle ScholarPubMed
Mezulis, A. H., Abramson, L. Y., Hyde, J. S., & Hankin, B. L. (2004). Is there a universal positivity bias in attributions? A meta-analytic review of individual, developmental, and cultural differences in the self-serving attributional bias. Psychological Bulletin, 130(5), 711–747. doi:10.1037/0033-2909.130.5.711.CrossRefGoogle Scholar
Moll, J., de Oliveira-Souza, R., Garrido, G. J., Bramati, I. E., Caparelli-Daquer, E. M., Paiva, M. L., … Grafman, J. (2007). The self as a moral agent: Linking the neural bases of social agency and moral sensitivity. Social Neuroscience, 2(3-4), 336–352. doi:10.1080/17470910701392024.CrossRefGoogle ScholarPubMed
Moll, J., Zahn, R., de Oliveira-Souza, R., Bramati, I. E., Krueger, F., Tura, B., … Grafman, J. (2011). Impairment of prosocial sentiments is associated with frontopolar and septal damage in frontotemporal dementia. Neuroimage, 54(2), 1735–1742.CrossRefGoogle ScholarPubMed
Montgomery, S. A., & Åsberg, M. (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry, 134(4), 382–389.CrossRefGoogle ScholarPubMed
Morey, R. A., McCarthy, G., Selgrade, E. S., Seth, S., Nasser, J. D., & LaBar, K. S. (2012). Neural systems for guilt from actions affecting self versus others. Neuroimage, 60(1), 683–692.CrossRefGoogle ScholarPubMed
O'Connor, L. E., Berry, J. W., Weiss, J., Bush, M., & Sampson, H. (1997). Interpersonal guilt: The development of a new measure. Journal of Clinical Psychology, 53(1), 73–89. doi:10.1002/(Sici)1097-4679(199701)53:1 < 73::Aid-Jclp10>3.0.Co;2-I.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
O'Connor, L. E., Berry, J. W., Weiss, J., & Gilbert, P. (2002). Guilt, fear, submission, and empathy in depression. Journal of Affective Disorders, 71(1–3), 19–27.CrossRefGoogle ScholarPubMed
Pobric, G., Lambon Ralph, M. A., & Zahn, R. (2016). Hemispheric specialization within the superior anterior temporal Cortex for social and nonsocial concepts. Journal of Cognitive Neuroscience, 28(3), 351–360. doi:10.1162/jocn_a_00902.CrossRefGoogle ScholarPubMed
Price, J. L., & Drevets, W. C. (2010). Neurocircuitry of mood disorders. Neuropsychopharm, 35(1), 192–216. doi:10.1038/npp.2009.104.CrossRefGoogle ScholarPubMed
Pulcu, E., Zahn, R., Moll, J., Trotter, P. D., Thomas, E. J., Juhasz, G., … Elliott, R. (2014). Enhanced subgenual cingulate response to altruistic decisions in remitted major depressive disorder. Neuroimage Clinical, 4, 701–710. doi:10.1016/j.nicl.2014.04.010.CrossRefGoogle ScholarPubMed
Ressler, K. J., & Mayberg, H. S. (2007). Targeting abnormal neural circuits in mood and anxiety disorders: From the laboratory to the clinic. Nature Neuroscience, 10(9), 1116–1124. doi:10.1038/nn1944.CrossRefGoogle ScholarPubMed
Robins, C. J., Ladd, J., Welkowitz, J., Blaney, P. H., Diaz, R., & Kutcher, G. (1994). The personal style inventory - preliminary validation studies of new measures of sociotropy and autonomy. Journal of Psychopathology and Behavioral Assessment, 16(4), 277–300. doi:10.1007/Bf02239408.CrossRefGoogle Scholar
Seara-Cardoso, A., Sebastian, C. L., McCrory, E., Foulkes, L., Buon, M., Roiser, J. P., & Viding, E. (2016). Anticipation of guilt for everyday moral transgressions: The role of the anterior insula and the influence of interpersonal psychopathic traits. Scientific Reports, 6, 36273. doi:10.1038/srep36273.CrossRefGoogle ScholarPubMed
Siegle, G. J., Carter, C. S., & Thase, M. E. (2006). Use of FMRI to predict recovery from unipolar depression with cognitive behavior therapy. American Journal of Psychiatry, 163(4), 735–738. doi:10.1176/appi.ajp.163.4.735.Google ScholarPubMed
Skipper, L. M., Ross, L. A., & Olson, I. R. (2011). Sensory and semantic category subdivisions within the anterior temporal lobes. Neuropsychologia, 49(12), 3419–3429. doi:10.1016/j.neuropsychologia.2011.07.033.CrossRefGoogle ScholarPubMed
Stevens, J. (2009). Applied multivariate statistics for the social sciences (5th ed.). New York: Routledge, Taylor & Francis Group.Google Scholar
Takahashi, H., Yahata, N., Koeda, M., Matsuda, T., Asai, K., & Okubo, Y. (2004). Brain activation associated with evaluative processes of guilt and embarrassment: An fMRI study. Neuroimage, 23(3), 967–974.CrossRefGoogle ScholarPubMed
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system : An approach to cerebral imaging. Stuttgart; New York: Georg Thieme.Google Scholar
Tangney, J. P., & Dearing, R. L. (2000). The test of self-conscious affect- 3 (TOSCA-3). Fairfax: George Mason University.Google Scholar
Tangney, J. P., Stuewig, J., & Mashek, D. J. (2007). Moral emotions and moral behavior. Annual Review of Psychology, 58, 345–372.CrossRefGoogle ScholarPubMed
Tangney, J. P., Wagner, P., & Gramzow, R. (1992). Proneness to shame, proneness to guilt, and psychopathology. Journal of Abnormal Psychology, 101(3), 469–478.CrossRefGoogle ScholarPubMed
Watson, D., Clark, L. A., & Tellegen, A. (1988). Development and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality and Social Psychology, 54(6), 1063–1070.CrossRefGoogle ScholarPubMed
Yang, K., & Girgus, J. S. (2019). Are women more likely than men are to care excessively about maintaining positive social relationships? A meta-analytic review of the gender difference in sociotropy. Sex Roles, 81(3), 157–172. doi:10.1007/s11199-018-0980-y.CrossRefGoogle Scholar
Zahn, R., de Oliveira-Souza, R., Bramati, I., Garrido, G., & Moll, J. (2009). Subgenual cingulate activity reflects individual differences in empathic concern. NeuroscienceLetters, 457(2), 107–110.Google ScholarPubMed
Zahn, R., De Oliveira-Souza, R., & Moll, J. (2020). Moral motivation and the basal forebrain. Neuroscience and Biobehavioral Reviews, 108, 207–217. doi:10.1016/j.neubiorev.2019.10.022.CrossRefGoogle ScholarPubMed
Zahn, R., Green, S., Beaumont, H., Burns, A., Moll, J., Caine, D., … Ralph, M. A. L. (2017). Frontotemporal lobar degeneration and social behaviour: Dissociation between the knowledge of its consequences and its conceptual meaning. Cortex, 93, 107–118. doi:10.1016/j.cortex.2017.05.009.CrossRefGoogle ScholarPubMed
Zahn, R., Lythe, K. E., Gethin, J. A., Green, S., Deakin, J. F., Workman, C., & Moll, J. (2015). Negative emotions towards others are diminished in remitted major depression. European Psychiatry, 30(4), 6. doi:10.1016/j.eurpsy.2015.02.005.CrossRefGoogle ScholarPubMed
Zahn, R., Lythe, K. E., Gethin, J. A., Green, S., Deakin, J. F., Young, A. H., & Moll, J. (2015). The role of self-blame and worthlessness in the psychopathology of major depressive disorder. Journal of Affective Disorders, 186, 337–341. doi::10.1016/j.jad.2015.08.001.CrossRefGoogle ScholarPubMed
Zahn, R., Moll, J., Krueger, F., Huey, E. D., Garrido, G., & Grafman, J. (2007). Social concepts are represented in the superior anterior temporal cortex. Proceedings of the National Academy of Sciences of the USA, 104(15), 6430–6435.CrossRefGoogle ScholarPubMed
Zahn, R., Moll, J., Paiva, M., Garrido, G., Krueger, F., Huey, E. D., & Grafman, J. (2009). The neural basis of human social values: Evidence from functional MRI. Cerebral Cortex, 19(2), 276–283. doi:10.1093/cercor/bhn080.CrossRefGoogle ScholarPubMed
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