Enhanced subgenual cingulate response to altruistic decisions in remitted major depressive disorder

NeuroImage: Clinical

Volumn 4, Issue , 2014, Pages 701-710

  Pulcu, Erdem ^a   Zahn, Roland ^a,c   Moll, Jorge ^e   Trotter, Paula D ^a   Thomas, Emma J ^a   Juhasz, Gabriella ^a,d   Deakin, J F William ^a   Anderson, Ian M ^a   Sahakian, Barbara J ^b   Elliott, Rebecca ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d SEMMELWEIS UNIVERSITY   (Hungary)

^e Labs D'or   (Brazil)

Author keywords

Charitable donation; Major depression; Reward processing; Striatum; Subgenual anterior cingulate

Indexed keywords

ADULT; ALTRUISM; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; CINGULATE GYRUS; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DECISION MAKING; DSM-IV-TR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBAL ASSESSMENT OF FUNCTIONING; HUMAN; INFERIOR FRONTAL GYRUS; MAJOR DEPRESSION; MALE; MONTGOMERY ASBERG DEPRESSION RATING SCALE; NERVE POTENTIAL; NUCLEAR MAGNETIC RESONANCE SCANNER; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REMISSION; REMITTED MAJOR DEPRESSIVE DISORDER; RESPONSE TIME; REWARD; SOCIAL PSYCHOLOGY; SUBGENUAL CINGULATE; BLOOD; IMAGE PROCESSING; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; PSYCHOLOGY; REACTION TIME; STATISTICAL MODEL; VASCULARIZATION; FUNCTIONAL NEUROIMAGING; GLOBUS PALLIDUS; SEPTUM PELLUCIDUM; SUBGENUAL CINGULATE CORTEX; VENTROMEDIAL PREFRONTAL CORTEX;

OXYGEN;

ADULT; ALTRUISM; DECISION MAKING; DEPRESSIVE DISORDER, MAJOR; FEMALE; GYRUS CINGULI; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; OXYGEN; PSYCHIATRIC STATUS RATING SCALES; REACTION TIME;

EID: 84899505482     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2014.04.010     Document Type: Article

References (68)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders fourth edition 2000 American Psychiatric Association Washington, DC
2. Amodio D.M., Frith C.D. Meeting of minds: the medial frontal cortex and social cognition Nature Reviews. Neuroscience 7 2006 268 277 10.1038/nrn1884 16552413
3. Andreoni J. Impure altruism and donations to public goods: a theory of warm-glow giving Economic Journal 100 1990 464 477 10.2307/2234133
4. Basile B., Mancini F., Macaluso E., Caltagirone C., Frackowiak R.S., Bozzali M. Deontological and altruistic guilt: evidence for distinct neurobiological substrates Human Brain Mapping 32 2011 229 239 10.1002/hbm.21009 20842749
5. Basile B., Mancini F., Macaluso E., Caltagirone C., Frackowiak R.S.J., Bozzali M. Deontological and altruistic guilt: evidence for distinct neurobiological substrates Human Brain Mapping 32 2011 229 239 20842749
6. Bhagwagar Z., Cowen P.J. 'It's not over when it's over': persistent neurobiological abnormalities in recovered depressed patients Psychological Medicine 38 2008 307 313 18444278 (Pubitemid 351311671)
7. Botteron K.N., Raichle M.E., Drevets W.C., Heath A.C., Todd R.D. Volumetric reduction in left subgenual prefrontal cortex in early onset depression Biological Psychiatry 51 2002 342 344 10.1016/S0006-3223(01)01280-X 11958786 (Pubitemid 34215000)
8. Botvinick M.M., Cohen J.D., Carter C.S. Conflict monitoring and anterior cingulate cortex: an update Trends in Cognitive Sciences 8 2004 539 546 10.1016/j.tics.2004.10.003 15556023 (Pubitemid 39536251)
9. Brett M., Anton J.-L., Valabregue R., Poline J.-B. Region of interest analysis using an SPM toolbox 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan 2002 Academic Press
10. Dichter G.S., Kozink R.V., Mcclernon F.J., Smoski M.J. Remitted major depression is characterized by reward network hyperactivation during reward anticipation and hypoactivation during reward outcomes Journal of Affective Disorders 136 2012 1126 1134 10.1016/j.jad.2011.09.048 22036801
11. Diekhof E.K., Kaps L., Falkai P., Gruber O. The role of the human ventral striatum and the medial orbitofrontal cortex in the representation of reward magnitude - an activation likelihood estimation meta-analysis of neuroimaging studies of passive reward expectancy and outcome processing Neuropsychologia 50 2012 1252 1266 10.1016/j.neuropsychologia.2012.02.007 22366111
12. Drevets W.C., Ongur D., Price J.L. Neuroimaging abnormalities in the subgenual prefrontal cortex: implications for the pathophysiology of familial mood disorders Molecular Psychiatry 3 1998 220 226 10.1038/sj.mp.4000370 9672897 (Pubitemid 28266331)
13. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., Raichle M.E. Subgenual prefrontal cortex abnormalities in mood disorders Nature 386 1997 824 827 10.1038/386824a0 9126739 (Pubitemid 27181254)
14. Drevets W.C., Savitz J. The subgenual anterior cingulate cortex in mood disorders CNS Spectrums 13 2008 663 681 18704022
15. Eaton W.W., Shao H., Nestadt G., Lee B.H., Bienvenu O.J., Zandi P. Population-based study of first onset and chronicity in major depressive disorder Archives of General Psychiatry 65 2008 513 520 10.1001/archpsyc.65.5. 513 18458203 (Pubitemid 351645047)
16. Eisenberg N. Emotion, regulation, and moral development Annual Review of Psychology 51 2000 665 697 10.1146/annurev.psych.51.1.665 10751984
17. Elliott R., Friston K.J., Dolan R.J. Dissociable neural responses in human reward systems Journal of Neuroscience: the Official Journal of the Society for Neuroscience 20 2000 6159 6165 10934265 (Pubitemid 30658409)
18. Elliott R., Lythe K., Lee R., Mckie S., Juhasz G., Thomas E.J., Downey D., Deakin J., Anderson I.M. Reduced medial prefrontal responses to social interaction images in remitted depression Archives of General Psychiatry 69 2012 37 45 10.1001/archgenpsychiatry.2011.139 22213787
19. Erk S., Spottke A., Meisen A., Wagner M., Walter H., Jessen F. Evidence of neuronal compensation during episodic memory in subjective memory impairment Archives of General Psychiatry 68 2011 845 852 10.1001/archgenpsychiatry.2011.80 21810648
20. Eshel N., Roiser J.P. Reward and punishment processing in depression Biological Psychiatry 68 2010 118 124 10.1016/j.biopsych.2010.01.027 20303067
21. Feldman Hall O., Dalgleish T., Thompson R., Evans D., Schweizer S., Mobbs D. Differential neural circuitry and self-interest in real vs hypothetical moral decisions Social Cognitive and Affective Neuroscience 7 2012 743 751 10.1093/scan/nss069 22711879
22. First M.B., Spitzer R.L., Miriam G., Williams J.B.W. Structured Clinical Interview for DSM-IV-TR Axis I Disorders Research Version, Non-patient Edition (SCID-I/NP) 2002 Biometrics Research, New York State Psychiatric Institute New York
23. Foster K.R., Wenseleers T., Ratnieks F.L. Kin selection is the key to altruism Trends in Ecology & Evolution 21 2006 57 60 10.1016/j.tree.2005.11. 020 16701471 (Pubitemid 43144374)
24. Fujiwara T. Is altruistic behavior associated with major depression onset? PloS One 4 2009 e4557 10.1371/journal.pone.0004557 19234611
25. Gramsbergen A. Neural compensation after early lesions: a clinical view of animal experiments Neuroscience and Biobehavioral Reviews 31 2007 1088 1094 10.1016/j.neubiorev.2007.10.002 18053874 (Pubitemid 350160953)
26. Green S., Lambon Ralph M.A., Moll J., Deakin J.F., Zahn R. Guilt-selective functional disconnection of anterior temporal and subgenual cortices in major depressive disorder Archives of General Psychiatry 69 2012 1014 1021 22638494
27. Green S., Matthew Lambon Ralph J.M.O.L.L., Deakin W., Zahn R. Guilt-selective functional disconnection of anterior temporal and subgenual cortices in major depressive disorder Archives of General Psychiatry 173 2012 1014 1021 22638494
28. Green S., Moll J., Deakin J.F.W., Hulleman J., Zahn R. Proneness to decreased negative emotions in major depressive disorder when blaming others rather than oneself Psychopathology 46 2013 34 44 10.1159/000338632 22890331
29. Greicius M.D., Flores B.H., Menon V., Glover G.H., Solvason H.B., Kenna H., Reiss A.L., Schatzberg A.F. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus Biological Psychiatry 62 2007 429 437 10.1016/j.biopsych.2006.09. 020 17210143 (Pubitemid 47284017)
30. Hamilton W.D. The evolution of altruistic behavior The American Naturalist 97 1963 354 356
31. Harbaugh W.T., Mayr U., Burghart D.R. Neural responses to taxation and voluntary giving reveal motives for charitable donations Science (New York, N.Y.) 316 2007 1622 1625 10.1126/science.1140738 17569866 (Pubitemid 46982036)
32. Hare T.A., Camerer C.F., Knoepfle D.T., O'Doherty J.P., Rangel A. Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition Journal of Neuroscience: the Official Journal of the Society for Neuroscience 30 2010 583 590 10.1523/JNEUROSCI.4089-09.2010 20071521
33. Hsu M., Anen C., Quartz S.R. The right and the good: distributive justice and neural encoding of equity and efficiency Science (New York, N.Y.) 320 2008 1092 1095 10.1126/science.1153651 18467558 (Pubitemid 351929553)
34. Immordino-Yang M.H., Mccoll A., Damasio H., Damasio A. Neural correlates of admiration and compassion Proceedings of the National Academy of Sciences of the United States of America 106 2009 8021 8026 10.1073/pnas.0810363106 19414310
35. Izuma K., Saito D.N., Sadato N. Processing of the incentive for social approval in the ventral striatum during charitable donation Journal of Cognitive Neuroscience 22 2010 621 631 10.1162/jocn.2009.21228 19320552
36. Kim S., Thibodeau R., Jorgensen R.S. Shame, guilt, and depressive symptoms: a meta-analytic review Psychological Bulletin 137 2011 68 96 10.1037/a0021466 21219057
37. Knutson B., Bhanji J.P., Cooney R.E., Atlas L.Y., Gotlib I.H. Neural responses to monetary incentives in major depression Biological Psychiatry 63 2008 686 692 10.1016/j.biopsych.2007.07.023 17916330 (Pubitemid 351329276)
38. Koenigs M., Tranel D. Irrational economic decision-making after ventromedial prefrontal damage: evidence from the ultimatum game Journal of Neuroscience: the Official Journal of the Society for Neuroscience 27 2007 951 956 10.1523/JNEUROSCI.4606-06.2007 17251437 (Pubitemid 46174516)
39. Lehmbeck J.T., Brassen S., Braus D.F., Weber-Fahr W. Subgenual anterior cingulate cortex alterations in late-onset depression are related to "pessimistic thoughts" American Journal of Geriatric Psychiatry: Official Journal of the American Association for Geriatric Psychiatry 16 2008 248 249 10.1097/JGP.0b013e318162a0c0 18310555
40. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets Neuroimage 19 2003 1233 1239 10.1016/S1053-8119(03)00169-1 12880848 (Pubitemid 36918259)
41. Mayberg H.S., Brannan S.K., Mahurin R.K., Jerabek P.A., Brickman J.S., Tekell J.L., Silva J.A., Mcginnis S., Glass T.G., Martin C.C., Fox P.T. Cingulate function in depression: a potential predictor of treatment response Neuroreport 8 1997 1057 1061 10.1097/00001756-199703030-00048 9141092 (Pubitemid 27152174)
42. Mayberg H.S., Brannan S.K., Tekell J.L., Silva J.A., Mahurin R.K., Mcginnis S., Jerabek P.A. Regional metabolic effects of fluoxetine in major depression: serial changes and relationship to clinical response Biological Psychiatry 48 2000 830 843 10.1016/S0006-3223(00)01036-2 11063978
43. Mayberg H.S., Lozano A.M., Voon V., Mcneely H.E., Seminowicz D., Hamani C., Schwalb J.M., Kennedy S.H. Deep brain stimulation for treatment-resistant depression Neuron 45 2005 651 660 10.1016/j.neuron.2005.02.014 15748841 (Pubitemid 40320700)
44. Moll J., Krueger F., Zahn R., Pardini M., de Oliveira-Souzat R., Grafman J. Human fronto-mesolimbic networks guide decisions about charitable donation Proceedings of the National Academy of Sciences of the United States of America 103 2006 15623 15628 10.1073/pnas.0604475103 17030808 (Pubitemid 44625642)
45. Moll J., Zahn R., de Oliveira-Souza R., Bramati I.E., Krueger F., Tura B., Cavanagh A.L., Grafman J. Impairment of prosocial sentiments is associated with frontopolar and septal damage in frontotemporal dementia Neuroimage 54 2011 1735 1742 10.1016/j.neuroimage.2010.08.026 20728544
46. Montgomery S.A., Asberg M. A new depression scale designed to be sensitive to change British Journal of Psychiatry: the Journal of Mental Science 134 1979 382 389 10.1192/bjp.134.4.382 444788 (Pubitemid 9136500)
47. Morey R.A., Mccarthy G., Selgrade E.S., Seth S., Nasser J.D., Labar K.S. Neural systems for guilt from actions affecting self versus others NeuroImage 60 2012 683 692 10.1016/j.neuroimage.2011.12.069 22230947
48. Nixon N., Liddle P., Nixon E., Worwood G., Liotti M., Palaniyappan L. Biological vulnerability to depression: linked structural and functional brain network findings British Journal of Psychiatry: the Journal of Mental Science 204 2014 283 289 24357570
49. O'Connor L.E., Berry J.W., Lewis T.B., Stiver D.J. Empathy-based pathogenic guilt, pathological altruism, and psychopathology Pathological Altruism 2012 Oxford Scholarship Online
50. O'Connor L.E., Berry J.W., Weiss J., Schweitzer D., Sevier M. Survivor guilt, submissive behaviour and evolutionary theory: the down-side of winning in social comparison British Journal of Medical Psychology 73 2000 519 530 10.1348/000711200160705 11140792 (Pubitemid 32005567)
51. Pulcu E., Lythe K., Elliott R., Green S., Moll J., Deakin J.F., Zahn R. Increased amygdala response to shame in remitted major depressive disorder PLoS ONE 9 2014 e86900 10.1371/journal.pone.0086900 24497992
52. Pulcu E., Zahn R., Elliott R. The role of self-blaming moral emotions in major depression and their impact on social-economical decision making Frontiers in Psychology 4 2013 1 17 23382719
53. Rilling J.K., King-Casas B., Sanfey A.G. The neurobiology of social decision-making Current Opinion in Neurobiology 18 2008 159 165 10.1016/j.conb.2008.06.003 18639633
54. Rushworth M.F., Buckley M.J., Behrens T.E., Walton M.E., Bannerman D.M. Functional organization of the medial frontal cortex Current Opinion in Neurobiology 17 2007 220 227 10.1016/j.conb.2007.03.001 17350820 (Pubitemid 46575241)
55. Sacchet M.D., Knutson B. Spatial smoothing systematically biases the localization of reward-related brain activity Neuroimage 66 2012 270 277 23110886
56. Sanfey A.G., Rilling J.K., Aronson J.A., Nystrom L.E., Cohen J.D. The neural basis of economic decision-making in the ultimatum game Science (New York, N.Y.) 300 2003 1755 1758 10.1126/science.1082976 12805551 (Pubitemid 36712573)
57. Schiller C.E., Minkel J., Smoski M.J., Dichter G.S. Remitted major depression is characterized by reduced prefrontal cortex reactivity to reward loss Journal of Affective Disorders 151 2013 756 762 10.1016/j.jad.2013.06.016 23835103
58. Schlaepfer T.E., Cohen M.X., Frick C., Kosel M., Brodesser D., Axmacher N., Joe A.Y., Kreft M., Lenartz D., Sturm V. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 33 2008 368 377 17429407 (Pubitemid 350243349)
59. Sescousse G., Caldú X., Segura B., Dreher J.-C. Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies Neuroscience and Biobehavioral Reviews 37 2013 681 696 23415703
60. Sheehan D.V., Lecrubier Y., Sheehan K.H., Amorim P., Janavs J., Weiller E., Hergueta T., Baker R., Dunbar G.C. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10 Journal of Clinical Psychiatry 59 1998 22 33 9881538 (Pubitemid 29001829)
61. Siegle G.J., Carter C.S., Thase M.E. Use of fMRI to predict recovery from unipolar depression with cognitive behavior therapy American Journal of Psychiatry 163 2006 735 738 10.1176/appi.ajp.163.4.735 16585452 (Pubitemid 44464587)
62. Tangney J.P., Stuewig J., Mashek D.J. Moral emotions and moral behavior Annual Review of Psychology 58 2007 345 372 10.1146/annurev.psych.56.091103. 070145 16953797
63. Tremblay L.K., Naranjo C.A., Graham S.J., Herrmann N., Mayberg H.S., Hevenor S., Busto U.E. Functional neuroanatomical substrates of altered reward processing in major depressive disorder revealed by a dopaminergic probe Archives of General Psychiatry 62 2005 1228 1236 10.1001/archpsyc.62.11.1228 16275810 (Pubitemid 41586922)
64. Walton M.E., Croxson P.L., Behrens T.E., Kennerley S.W., Rushworth M.F. Adaptive decision making and value in the anterior cingulate cortex Neuroimage 36 Suppl 2 2007 T142 T154 17499161
65. Wright K. Generosity Versus Altruism: Philanthropy and Charity in the US and UK 2002 Centre for Civil Society
66. Zahn R., de Oliveira-Souza R., Bramati I., Garrido G., Moll J. Subgenual cingulate activity reflects individual differences in empathic concern Neuroscience Letters 457 2009 107 110 10.1016/j.neulet.2009.03.090 19429173
67. Zahn R., Moll J., Paiva M., Garrido G., Krueger F., Huey E.D., Grafman J. The neural basis of human social values: evidence from functional MRI Cerebral Cortex (New York, N.Y.: 1991) 19 2009 276 283 10.1093/cercor/bhn080 18502730
68. Zahn R., Moll J., Paiva M.M.F., Garrido G., Krueger F., Huey E.D., Grafman J. The neural basis of human social values: evidence from functional MRI Cerebral Cortex (New York, N.Y.: 1991) 19 2009 276 283 10.1093/cercor/bhn080 18502730