Divergent relationship of depression severity to social reward responses among patients with bipolar versus unipolar depression

Psychiatry Research - Neuroimaging

Volumn 254, Issue , 2016, Pages 18-25

  Sharma, Anup ^a   Satterthwaite, Theodore D ^a   Vandekar, Lillie ^a   Katchmar, Natalie ^a   Daldal, Aylin ^a   Ruparel, Kosha ^a   Elliott, Mark A ^a   Baldassano, Claudia ^a   Thase, Michael E ^a   Gur, Raquel E ^a   Kable, Joseph W ^a   Wolf, Daniel H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Magnetic resonance imaging; Mood disorders; Neuroimaging

Indexed keywords

ADULT; ANGER; ARTICLE; BIPOLAR DEPRESSION; BLUNTED AFFECT; BOLD SIGNAL; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HAPPINESS; HUMAN; IMAGE ANALYSIS; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; NUCLEAR MAGNETIC RESONANCE SCANNER; ORBITAL CORTEX; PRIORITY JOURNAL; REWARD; SOCIAL PSYCHOLOGY; SOCIAL REWARD; VENTRAL STRIATUM; VENTROMEDIAL PREFRONTAL CORTEX; BIPOLAR DISORDER; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PERCEPTION; PREFRONTAL CORTEX;

ADULT; BIPOLAR DISORDER; DEPRESSIVE DISORDER, MAJOR; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PREFRONTAL CORTEX; REWARD; SOCIAL PERCEPTION; VENTRAL STRIATUM;

EID: 84973442937     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2016.06.003     Document Type: Article

References (76)

1. Abler B., Erk S., Walter H. Human reward system activation is modulated by a single dose of olanzapine in healthy subjects in an event-related, double-blind, placebo-controlled fmri study. Psychopharmacology 2007, 191:823-833.
2. Abler B., Greenhouse I., Ongur D., Walter H., Heckers S. Abnormal reward system activation in mania. Neuropsychopharmacology 2008, 33:2217-2227.
3. Almeida J.R., Versace A., Mechelli A., Hassel S., Quevedo K., Kupfer D.J., Phillips M.L. Abnormal amygdala-prefrontal effective connectivity to happy faces differentiates bipolar from major depression. Biol. Psychiatry 2009, 66:451-459.
4. Almeida J.R., Phillips M.L. Distinguishing between unipolar depression and bipolar depression: current and future clinical and neuroimaging perspectives. Biol. Psychiatry 2013, 73:111-118.
5. Ayduk O., Downey G., Kim M. Rejection sensitivity and depressive symptoms in women. Pers. Social Psychol. Bull. 2001, 27:868-877.
6. Bartra O., McGuire J.T., Kable J.W. The valuation system: a coordinate-based meta-analysis of BOLD fmri experiments examining neural correlates of subjective value. NeuroImage 2013, 76:412-427.
7. Beck A.T., Steer R.A., Ball R., Ranieri W. Comparison of beck depression inventories -IA and -II in psychiatric outpatients. J. Pers. Assess. 1996, 67:588-597.
8. Bermpohl F., Kahnt T., Dalanay U., Hägele C., Sajonz B., Wegner T., Stoy M., Adli M., Kruger S., Wrase J., Strohle A., Bauer M., Heinz A. Altered representation of expected value in the orbitofrontal cortex in mania. Hum. Brain Mapp. 2010, 31:958-969.
9. Bertocci M.A., Bebko G.M., Mullin B.C., Langenecker S.A., Ladouceur C.D., Almeida J.R., Phillips M.L. Abnormal anterior cingulate cortical activity during emotional n-back task performance distinguishes bipolar from unipolar depressed females. Psychol. Med. 2012, 42:1417-1428.
10. Bosc M. Assessment of social functioning in depression. Compr. Psychiatry 2000, 41:63-69.
11. Bilek E., Ruf M., Schäfer A., Akdeniz C., Calhoun V.D., Schmahl C., Demanuele C., Tost H., Kirsch P., Meyer-Lindenberg A. Information flow between interacting human brains: Identification, validation, and relationship to social expertise. Proc. Natl. Acad. Sci. 2015, 112:5207-5212.
12. Boyce P., Hickie I., Parker G., Mitchell P., Wilhelm K., Brodaty H. Interpersonal sensitivity and the one-year outcome of a depressive episode. Aust. N. Z. J. Psychiatry 1992, 26:156-161.
13. Carver C.S., Harmon-Jones E. Anger is an approach-related affect: evidence and implications. Psychol. Bull. 2009, 135:183.
14. Caseras X., Lawrence N.S., Murphy K., Wise R.G., Phillips M.L. Ventral striatum activity in response to reward: Differences between bipolar I and II disorders. Am. J. Psychiatry 2013, 170:533-541.
15. Chase H.W., Nusslock R., Almeida J.R.C., Forbes E.E., LaBarbara E.J., Phillips M.L. Dissociable patterns of abnormal frontal cortical activation during anticipation of an uncertain reward or loss in bipolar versus major depression. Bipolar Disord. 2013, 15:839-854.
16. Cohen A.N., Hammen C., Henry R.M., Daley S.E. Effects of stress and social support on recurrence in bipolar disorder. J. Affect Disord. 2004, 82:143-147.
17. Connolly K.R., Thase M.E. The clinical management of bipolar disorder: A review of evidence-based guidelines. Prim. Care Companion CNS Disord. 2011, 13. (pii: PCC.10r01097.).
18. Cox A., Kohls G., Naples A.J., Mukerji C.E., Coffman M.C., Rutherford H.J.V., Mayes L.C., McPartland J.C. Diminished social reward anticipation in the broad autism phenotype as revealed by event-related brain potentials. Soc. Cogn. Affect. Neurosci. 2015, 10.1093/scan/nsv024.
19. Cremers H.R., Veer I.M., Spinhoven P., Rombouts S.A., Roelofs K. Neural sensitivity to social reward and punishment anticipation in social anxiety disorder. Front Behav. Neurosci. 2015, 8. 10.3389/fnbeh.2014.00439.
20. Delgado M.R., Nystrom L.E., Fissell C., Noll D.C., Fiez J.A. Tracking the hemodynamic responses to reward and punishment in the striatum. J. Neurophysiol. 2000, 84:3072-3077.
21. Delmonte S., Balsters J.H., McGrath J., Fitzgerald J., Brennan S., Fagan A.J., Gallagher L. Social and monetary reward processing in autism spectrum disorders. Mol. Autism 2012, 10.1186/2040-2392-3-7.
22. Delvecchio G., Fossati P., Boyer P., Brambilla P., Falkai P., Gruber O., Hietala J., Lawrie S.M., Martinot J.L., McIntosh A.M., Meisenzahl E., Frangou S. Common and distinct neural correlates of emotional processing in bipolar disorder and major depressive disorder: a voxel-based meta-analysis of functional magnetic resonance imaging studies. Eur. Neuropsychopharmacol. 2012, 22:100-113.
23. De Silva M.J., Cooper S., Li H.L., Lund C., Patel V. Effect of psychosocial interventions on social functioning in depression and schizophrenia: meta-analysis. Br. J. Psychiatry 2013, 202:253-260.
24. Dichter G.S., Richey J.A., Rittenberg A.M., Sabatino A., Bodfish J.W. Reward circuitry function in autism during face anticipation and outcomes. J. Autism Dev. Disord. 2012, 42:147-160.
25. Doshi J., Erus G., Ou Y., Gaonkar B., Davatzikos C. Multi-atlas skull-stripping. Acad. Radiol. 2013, 20:1566-1576.
26. Ehnvall A., Mitchell P.B., Hadzi-Pavlovic D., Parker G., Frankland A., Loo C., Breakspear M., Wright A., Roberts G., Lau P., Perich T. Rejection sensitivity and pain in bipolar versus unipolar depression. Bipolar Disord. 2014, 16:190-198.
27. Ferrari A.J., Charlson F.J., Norman R.E., Patten S.B., Freedman G., Murray C.J., Vos T., Whiteford H.A. Burden of depressive disorders by country, sex, age, and year: findings from the global burden of disease study 2010. PLoS Med. 2013, 10:e1001547.
28. Flores A., Münte T.F., Doñamayor N. Event-related EEG responses to anticipation and delivery of monetary and social reward. Biol. Psychol. 2015, 10.1016/j.biopsycho.2015.04.005.
29. Forte A., Baldessarini R.J., Tondo L., Vázquez G.H., Pompili M., Girardi P. Long-term morbidity in bipolar-i, bipolar-ii, and unipolar major depressive disorders. J. Affect Disord. 2015, 178:71-78.
30. Foulkes L., Bird G., Gökçen E., McCrory E., Viding E. Common and distinct impacts of autistic traits and alexithymia on social reward. PLoS One 2015, 10:e0121018.
31. Fournier J.C., Keener M.T., Almeida J., Kronhaus D.M., Phillips M.L. Amygdala and whole-brain activity to emotional faces distinguishes major depressive disorder and bipolar disorder. Bipolar Disord. 2013, 15:741-752.
32. Ghaemi S.N., Rosenquist K.J., Ko J.Y., Baldassano C.F., Kontos N.J., Baldessarini R.J. Antidepressant treatment in bipolar versus unipolar depression. Am. J. Psychiatry 2004, 161:163-165.
33. Greve D.N., Fischl B. Accurate and robust brain image alignment using boundary-based registration. NeuroImage 2009, 48:63-72.
34. Groppe S.E., Gossen A., Rademacher L., Hahn A., Westphal L., Gründer G., Spreckelmeyer K.N. Oxytocin influences processing of socially relevant cues in the ventral tegmental area of the human brain. Biol. Psychiatry 2013, 74:172-179.
35. Grotegerd D., Stuhrmann A., Kugel H., Schmidt S., Redlich R., Zwanzger P., Rauch A.V., Heindel W., Zwitserlood P., Arolt V., Suslow T., Dannlowski U. Amygdala excitability to subliminally presented emotional faces distinguishes unipolar and bipolar depression: An fmri and pattern classification study. Hum. Brain Mapp. 2014, 35:2995-3007.
36. Gunaydin, L.A., Deisseroth, K., 2015. Dopaminergic Dynamics Contributing to Social Behavior, In: Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press.
37. Gur R.C., Sara R., Hagendoorn M., Marom O., Hughett P., Macy L., Turner T., Bajcsy R., Posner A., Gur R.E. A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. J. Neurosci. Methods 2002, 115:137-143.
38. Hägele C., Schlagenhauf F., Rapp M., Sterzer P., Beck A., Bermpohl F., Stoy M., Strohle A., Wittchen H.U., Dolan R.J., Heinz A. Dimensional psychiatry: Reward dysfunction and depressive mood across psychiatric disorders. Psychopharmacol. (Berl. ) 2015, 232:331-341.
39. Hassel S., Almeida J.R., Kerr N., Nau S., Ladouceur C.D., Fissell K., Kuper D.J., Phillips M.L. Elevated striatal and decreased dorsolateral prefrontal cortical activity in response to emotional stimuli in euthymic bipolar disorder: no associations with psychotropic medication load. Bipolar Disord. 2008, 10:916-927.
40. Henderson S.E., Vallejo A.I., Ely B.A., Kang G., Krain Roy A., Pine D.S., Stern E.R., Gabbay V. The neural correlates of emotional face-processing in adolescent depression: a dimensional approach focusing on anhedonia and illness severity. Psychiatry Res. 2014, 224:234-241.
41. Izuma K., Saito D.N., Sadato N. Processing of social and monetary rewards in the human striatum. Neuron 2008, 58:284-294.
42. Jenkinson M., Beckmann C.F., Behrens T.E., Woolrich M.W., Smith S.M. FSL. NeuroImage 2012, 62:782-790.
43. Johnson S.L., Kizer A. Bipolar and unipolar depression: A comparison of clinical phenomenology and psychosocial predictors. Handbook of Depression 2002, 141-165. Guilford Press, New York. I.H. Gotlib, C.L. Hammen (Eds.).
44. Johnson S.L., Edge M.D., Holmes M.K., Carver C.S. The behavioral activation system and mania. Annu. Rev. Clin. Psychol. 2012, 8:243.
45. Judd L.L., Akiskal H.S., Schettler P.J., Endicott J., Maser J., Solomon D.A., Leon A.C., Rice J.A., Keller M.B. The long-term natural history of the weekly symptomatic status of bipolar I disorder. Arch. General. Psychiatry 2002, 59:530-537.
46. Kable J.W., Glimcher P.W. The neurobiology of decision: Consensus and controversy. Neuron 2009, 63:733-745.
47. Knutson B., Adams C.M., Fong G.W., Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J. Neurosci. 2001, 21:RC159.
48. Kohler C.G., Turner T.H., Bilker W.B., Brensinger C.M., Siegel S.J., Kanes S.J., Gur R.E., Gur R.C. Facial emotion recognition in schizophrenia: Intensity effects and error pattern. Am. J. Psychiatry 2003, 160:1768-1774.
49. Kohls G., Schulte-Rüther M., Nehrkorn B., Müller K., Fink G.R., Kamp-Becker I., Herpertz-Dahlmann B., Schultz R.T., Konrad K. Reward system dysfunction in autism spectrum disorders. Soc. Cogn. Affect Neurosci. 2013, 8:565-572.
50. Li C., Gore J.C., Davatzikos C. Multiplicative intrinsic component optimization (MICO) for MRI bias field estimation and tissue segmentation. Magn. Reson Imaging 2014, 32:913-923.
51. Linke J., King A.V., Rietschel M., Strohmaier J., Hennerici M., Gass A., Meyer-Lindenberg A., Wessa M. Increased medial orbitofrontal and amygdala activation: Evidence for a systems-level endophenotype of bipolar I disorder. Am. J. Psychiatry 2012, 169:316-325.
52. Miklowitz D.J., Johnson S.L. Social and familial factors in the course of bipolar disorder: basic processes and relevant interventions. Clin. Psychol. 2009, 16:281-296.
53. Ng T.H., Johnson S.L. Rejection sensitivity is associated with quality of life, psychosocial outcome, and the course of depression in euthymic patients with bipolar I disorder. Cognit. Ther. Res. 2013, 37:1169-1178.
54. Nusslock R., Almeida J.R., Forbes E.E., Versace A., Frank E., Labarbara E.J., Klein C.R., Phillips M.L. Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults. Bipolar Disord. 2012, 14:249-260.
55. Ou Y., Sotiras A., Paragios N., Davatzikos C. DRAMMS: Deformable registration via attribute matching and mutual-saliency weighting. Med. Image Anal. 2011, 15:622-639.
56. Peters J., Bromberg U., Schneider S., Brassen S., Menz M., Banaschewski T., Conrod P.J., Flor H., Gallinat J., Garavan H., Heinz A., Itterman B., Lathrop M., Martinot J.L., Paus T., Poline J.B., Robbins T.W., Rietschel M., Smolka M., Ströhle A., Struve M., Loth E., Schumann G., Büchel C., Consortium I.M.A.G.E.N. Lower ventral striatal activation during reward anticipation in adolescent smokers. Am. J. Psychiatry 2011, 168:540-549.
57. Phillips M.L., Swartz H.A. A critical appraisal of neuroimaging studies of bipolar disorder: Toward a new conceptualization of underlying neural circuitry and a road map for future research. Am. J. Psychiatry 2014, 171:829-843.
58. Pizzagalli D.A., Jahn A.L., O'Shea J.P. Toward an objective characterization of an anhedonic phenotype: a signal-detection approach. Biol. Psychiatry 2005, 57:319-327.
59. Pizzagalli D.A., Iosifescu D., Hallett L.A., Ratner K.G., Fava M. Reduced hedonic capacity in major depressive disorder: evidence from a probabilistic reward task. J. Psychiatr. Res. 2008, 43:76-87.
60. Pizzagalli D.A., Holmes A.J., Dillon D.G., Goetz E.L., Birk J.L., Bogdan R., Dougherty D.D., Iosifescu D.V., Rauch S.L., Fava M. Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. Am. J. Psychiatry 2009, 166:702-710.
61. Post R.M. The impact of bipolar depression. J. Clin. Psychiatry 2005, 66:5-10.
62. Posternak M.A., Zimmerman M. Symptoms of atypical depression. Psychiatry Res. 2001, 104:175-181.
63. Redlich R., Dohm K., Grotegerd D., Opel N., Zwitserlood P., Heindel W., Arolt V., Kugel A., Dannlowski U. Reward processing in unipolar and bipolar depression: a functional MRI study. Neuropsychopharmacology 2015, 40:2623-2631.
64. Ruff C.C., Fehr E. The neurobiology of rewards and values in social decision making. Nat. Rev. Neurosci. 2014, 15:549-562.
65. Satterthwaite T.D., Green L., Myerson J., Parker J., Ramaratnam M., Buckner R.L. Dissociable but inter-related systems of cognitive control and reward during decision making: Evidence from pupillometry and event-related fmri. NeuroImage 2007, 37:1017-1031.
66. Satterthwaite T.D., Kable J.W., Vandekar L., Katchmar N., Bassett D.S., Baldassano C.F., Ruparel K., Elliott M.A., Sheline Y.I., Gur R.C., Gur R.E., Davatzikos C., Leibenluft E., Thase M.E., Wolf D.H. Common and dissociable dysfunction of the reward system in bipolar and unipolar depression. Neuropsychopharmacology 2015, 40:2258-2268.
67. Scott-Van Zeeland A.A., Dapretto M., Ghahremani D.G., Poldrack R.A., Bookheimer S.Y. Reward processing in autism. Autism Res. 2010, 3:53-67.
68. Sescousse G., Redouté J., Dreher J.C. The architecture of reward value coding in the human orbitofrontal cortex. J. Neurosci. 2010, 30:13095-13104.
69. Simon J.J., Biller A., Walther S., Roesch-Ely D., Stippich C., Weisbrod M., Kaiser S. Neural correlates of reward processing in schizophrenia--relationship to apathy and depression. Schizophr. Res. 2010, 118:154-161.
70. Smith D.V., Hayden B.Y., Truong T.K., Song A.W., Platt M.L., Huettel S.A. Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J. Neurosci. 2010, 30:2490-2495.
71. Smoski M.J., Felder J., Bizzell J., Green S.R., Ernst M., Lynch T.R., Dichter G.S. FMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. J. Affect Disord. 2009, 118:69-78.
72. Steele J.D., Kumar P., Ebmeier K.P. Blunted response to feedback information in depressive illness. Brain 2007, 130:2367-2374.
73. Stoy M., Schlagenhauf F., Sterzer P., Bermpohl F., Hägele C., Suchotzki K., Schmack K., Wrase J., Ricken R., Knutson B., Adli M., Bauer M., Heinz A., Ströhle A. Hyporeactivity of ventral striatum towards incentive stimuli in unmedicated depressed patients normalizes after treatment with escitalopram. J. Psychopharmacol. 2012, 26:677-688.
74. Whitton A.E., Treadway M.T., Pizzagalli D.A. Reward processing dysfunction in major depression, bipolar disorder and schizophrenia. Curr. Opin. Psychiatry 2015, 28:7-12.
75. Wolf D.H., Satterthwaite T.D., Kantrowitz J.J., Katchmar N., Vandekar L., Elliott M.A., Ruparel K. Amotivation in schizophrenia: Integrated assessment with behavioral, clinical, and imaging measures. Schizophr. Bull. 2014, 40:1328-1337.
76. Woolrich M.W., Ripley B.,D., Brady M., Smith S.M. Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage 2001, 14:1370-1386.