Microstructural abnormalities in subcortical reward circuitry of subjects with major depressive disorder

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Blood, Anne J ^a   Iosifescu, Dan V ^a,b   Makris, Nikos ^a   Perlis, Roy H ^a   Kennedy, David N ^a   Dougherty, Darin D ^a   Kim, Byoung Woo ^a   Lee, Myung Joo ^a   Wu, Shirley ^a   Lee, Sang ^a   Calhoun, Jesse ^a   Hodge, Steven M ^a   Fava, Maurizio ^a   Rosen, Bruce R ^a   Smoller, Jordan W ^a   Gasic, Gregory P ^a   Breiter, Hans C ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; AMYGDALOFUGAL PATHWAY; ANHEDONIA; ANTERIOR CINGULATE CORTEX; ANXIETY; ARTICLE; AVERSION; BRAIN REGION; CALCARINE CORTEX; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; DISEASE SEVERITY; EMOTION; FEMALE; FRACTIONAL ANISOTROPY; GRAY MATTER; HUMAN; HYPOTHALAMUS NUCLEUS; LEFT HEMISPHERE; MAJOR DEPRESSION; MALE; MEDIAL DORSAL MIDBRAIN; MEDIAL FOREBRAIN BUNDLE; MESENCEPHALON; ORBITAL CORTEX; PARACINGULATE CORTEX; PERIAQUEDUCTAL GRAY MATTER; PREFRONTAL CORTEX; PREMOTOR CORTEX; PSYCHOMOTOR DISORDER; REWARD; RIGHT HEMISPHERE; SADNESS; SUBGENUAL CORTEX; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM; WHITE MATTER; ANISOTROPY; AVOIDANCE BEHAVIOR; BRAIN MAPPING; COHORT ANALYSIS; CONGENITAL MALFORMATION; METHODOLOGY; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT; ANISOTROPY; AVOIDANCE LEARNING; BRAIN MAPPING; COHORT STUDIES; DEPRESSIVE DISORDER, MAJOR; FEMALE; HUMANS; MALE; MEDIAL FOREBRAIN BUNDLE; MIDDLE AGED; REWARD; SUBSTANTIA NIGRA; VENTRAL TEGMENTAL AREA; YOUNG ADULT;

EID: 78649723125     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013945     Document Type: Article

References (95)

1. Breiter HC, Gasic GP (2004) A General Circuitry of Reward/Aversion and Its Implications for Neuropsychiatric Illness. In: M Gazzaniga, ed. The Cognitive Neurosciences MIT Press. pp 1043-1065.
2. Pizzagalli DA, Holmes AJ, Dillon DG, Goetz EL, Birk JL, et al. (2009) Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. Am J Psychiatry 166: 702-710.
3. Forbes EE (2009) Where's the fun in that? Broadening the focus on reward function in depression. Biol Psychiatry 66: 199-200.
4. McCabe C, Cowen PJ, Harmer CJ (2009) Neural representation of reward in recovered depressed patients. Psychopharmacology (Berl) 205: 667-677.
5. Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, et al. (2007) Deep Brain Stimulation to Reward Circuitry Alleviates Anhedonia in Refractory Major Depression. Neuropsychopharmacology.
6. Tremblay LK, Naranjo CA, Graham SJ, Herrmann N, Mayberg HS, et al. (2005) Functional neuroanatomical substrates of altered reward processing in major depressive disorder revealed by a dopaminergic probe. Arch Gen Psychiatry 62: 1228-1236.
7. Nestler EJ, Carlezon WA Jr. (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59: 1151-1159.
8. Breiter HC, Rosen BR (1999) Functional magnetic resonance imaging of brain reward circuitry in the human. Ann N Y Acad Sci 877: 523-547.
9. Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, et al. (1996) Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17: 875-887.
10. Blood AJ, Zatorre RJ, Bermudez P, Evans AC (1999) Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci 2: 382-387.
11. Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P (2001) Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron 30: 619-639.
12. Becerra L, Breiter HC, Wise R, Gonzalez RG, Borsook D (2001) Reward circuitry activation by noxious thermal stimuli. Neuron 32: 927-946.
13. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA (2000) Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84: 3072-3077.
14. Jensen J, McIntosh AR, Crawley AP, Mikulis DJ, Remington G, et al. (2003) Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron 40: 1251-1257.
15. Roitman MF, Wheeler RA, Carelli RM (2005) Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 45: 587-597.
16. Menon M, Jensen J, Vitcu I, Graff-Guerrero A, Crawley A, et al. (2007) Temporal difference modeling of the blood-oxygen level dependent response during aversive conditioning in humans: effects of dopaminergic modulation. Biol Psychiatry 62: 765-772.
17. Diaconescu AO, Menon M, Jensen J, Kapur S, McIntosh AR Dopamineinduced changes in neural network patterns supporting aversive conditioning. Brain Res 1313: 143-161.
18. Matsumoto M, Hikosaka O (2009) Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459: 837-841.
19. Leknes S, Tracey I (2008) A common neurobiology for pain and pleasure. Nat Rev Neurosci 9: 314-320.
20. Levita L, Hare TA, Voss HU, Glover G, Ballon DJ, et al. (2009) The bivalent side of the nucleus accumbens. Neuroimage 44: 1178-1187.
21. Carlezon WA Jr., Thomas MJ (2009) Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56 Suppl 1: 122-132.
22. Kim BW, Kennedy DN, Lehar J, Lee MJ, Blood AJ, et al. Recurrent, robust and scalable patterns underlie human approach and avoidance. PLoS One 5: e10613.
23. Bogdan R, Pizzagalli DA (2006) Acute stress reduces reward responsiveness: implications for depression. Biol Psychiatry 60: 1147-1154.
24. Breiter HC, Gasic GP, Makris, N (2006) Imaging the neural systems for motivated behavior and their dysfunction in neuropsychiatric illness. In: Deisboeck T, Kresh J, eds. Complex systems science in biomedicine. New York: Springer Verlag. pp 763-810.
25. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, et al. (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311: 864-868.
26. Olds J, Milner P (1954) Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 47: 419-427.
27. Wise RA, Bozarth MA (1985) Brain mechanisms of drug reward and euphoria. Psychiatr Med 3: 445-460.
28. Wise RA (1978) Catecholamine theories of reward: a critical review. Brain Res 152: 215-247.
29. Manji HK, Drevets WC, Charney DS (2001) The cellular neurobiology of depression. Nat Med 7: 541-547.
30. Breiter HC, Gollub RL, Weisskoff RM, Kennedy DN, Makris N, et al. (1997) Acute effects of cocaine on human brain activity and emotion. Neuron 19: 591-611.
31. Milak MS, Parsey RV, Lee L, Oquendo MA, Olvet DM, et al. (2009) Pretreatment regional brain glucose uptake in the midbrain on PET may predict remission from a major depressive episode after three months of treatment. Psychiatry Res 173: 63-70.
32. Wacker J, Dillon DG, Pizzagalli DA (2009) The role of the nucleus accumbens and rostral anterior cingulate cortex in anhedonia: integration of resting EEG, fMRI, and volumetric techniques. Neuroimage 46: 327-337.
33. Nobuhara K, Okugawa G, Sugimoto T, Minami T, Tamagaki C, et al. (2006) Frontal white matter anisotropy and symptom severity of late-life depression: a magnetic resonance diffusion tensor imaging study. J Neurol Neurosurg Psychiatry 77: 120-122.
34. Drevets WC, Price JL, Simpson JR, Jr., Todd RD, Reich T, et al. (1997) Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386: 824-827.
35. Drevets WC, Ongur D, Price JL (1998) Reduced glucose metabolism in the subgenual prefrontal cortex in unipolar depression. Mol Psychiatry 3: 190-191.
36. Taylor WD, MacFall JR, Payne ME, McQuoid DR, Provenzale JM, et al. (2004) Late-life depression and microstructural abnormalities in dorsolateral prefrontal cortex white matter. Am J Psychiatry 161: 1293-1296.
37. Keedwell PA, Andrew C, Williams SC, Brammer MJ, Phillips ML (2005) The neural correlates of anhedonia in major depressive disorder. Biol Psychiatry 58: 843-853.
38. Alexopoulos GS, Kiosses DN, Choi SJ, Murphy CF, Lim KO (2002) Frontal white matter microstructure and treatment response of late-life depression: a preliminary study. Am J Psychiatry 159: 1929-1932.
39. Bae JN, MacFall JR, Krishnan KR, Payne ME, Steffens DC, et al. (2006) Dorsolateral prefrontal cortex and anterior cingulate cortex white matter alterations in late-life depression. Biol Psychiatry 60: 1356-1363.
40. Frodl T, Meisenzahl EM, Zetzsche T, Born C, Groll C, et al. (2002) Hippocampal changes in patients with a first episode of major depression. Am J Psychiatry 159: 1112-1118.
41. Mintun MA, Sheline YI, Moerlein SM, Vlassenko AG, Huang Y, et al. (2004) Decreased hippocampal 5-HT2A receptor binding in major depressive disorder: in vivo measurement with [18F]altanserin positron emission tomography. Biol Psychiatry 55: 217-224.
42. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW (1996) Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci U S A 93: 3908-3913.
43. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, et al. (2000) Hippocampal volume reduction in major depression. Am J Psychiatry 157: 115-118.
44. Saxena S, Brody AL, Ho ML, Alborzian S, Ho MK, et al. (2001) Cerebral metabolism in major depression and obsessive-compulsive disorder occurring separately and concurrently. Biol Psychiatry 50: 159-170.
45. Edwards E, Kornrich W, van Houtten P, Henn FA (1992) In vitro neurotransmitter release in an animal model of depression. Neurochem Int 21: 29-35.
46. Drevets WC, Price JL, Bardgett ME, Reich T, Todd RD, et al. (2002) Glucose metabolism in the amygdala in depression: relationship to diagnostic subtype and plasma cortisol levels. Pharmacol Biochem Behav 71: 431-447.
47. Frodl T, Meisenzahl E, Zetzsche T, Bottlender R, Born C, et al. (2002) Enlargement of the amygdala in patients with a first episode of major depression. Biol Psychiatry 51: 708-714.
48. Mayberg HS (2003) Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. Br Med Bull 65: 193-207.
49. Fava M, Martinez JM, Greist J, Marangell LB, Brown E, et al. (2007) The efficacy and tolerability of duloxetine in the treatment of anxious versus nonanxious depression: a post-hoc analysis of an open-label outpatient study. Ann Clin Psychiatry 19: 187-195.
50. Sobin C, Sackeim HA (1997) Psychomotor symptoms of depression. Am J Psychiatry 154: 4-17.
51. Dougherty DD, Weiss AP, Cosgrove GR, Alpert NM, Cassem EH, et al. (2003) Cerebral metabolic correlates as potential predictors of response to anterior cingulotomy for treatment of major depression. J Neurosurg 99: 1010-1017.
52. Langguth B, Wiegand R, Kharraz A, Landgrebe M, Marienhagen J, et al. (2007) Pre-treatment anterior cingulate activity as a predictor of antidepressant response to repetitive transcranial magnetic stimulation (rTMS). Neuro Endocrinol Lett 28: 633-638.
53. Grimm S, Beck J, Schuepbach D, Hell D, Boesiger P, et al. (2008) Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: an fMRI study in severe major depressive disorder. Biol Psychiatry 63: 369-376.
54. Surguladze S, Brammer MJ, Keedwell P, Giampietro V, Young AW, et al. (2005) A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biol Psychiatry 57: 201-209.
55. Phillips ML, Drevets WC, Rauch SL, Lane R (2003) Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biol Psychiatry 54: 515-528.
56. Abercrombie HC, Schaefer SM, Larson CL, Oakes TR, Lindgren KA, et al. (1998) Metabolic rate in the right amygdala predicts negative affect in depressed patients. Neuroreport 9: 3301-3307.
57. Fava M, Uebelacker LA, Alpert JE, Nierenberg AA, Pava JA, et al. (1997) Major depressive subtypes and treatment response. Biol Psychiatry 42: 568-576.
58. Treadway MT, Buckholtz JW, Schwartzman AN, Lambert WE, Zald DH (2009) Worth the 'EEfRT'? The effort expenditure for rewards task as an objective measure of motivation and anhedonia. PLoS One 4: e6598.
59. First MB, Spitzer RL, Gibbon M, Williams JBW (1996) Structured Clinical Interview for DSM-IV Axis I Disorders. Patient edition (SCID-I/P) ed. New York: Biometrics Research Department, New York State Psychiatric Institute.
60. Hamilton M (1967) Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol 6: 278-296.
61. van der Kouwe AJ, Benner T, Fischl B, Schmitt F, Salat DH, et al. (2005) Online automatic slice positioning for brain MR imaging. Neuroimage 27: 222-230.
62. Deichmann R, Gottfried JA, Hutton C, Turner R (2003) Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19: 430-441.
63. Salat DH, Tuch DS, Greve DN, van der Kouwe AJ, Hevelone ND, et al. (2005) Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiol Aging 26: 1215-1227.
64. Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36: 893-906.
65. Boska MD, Hasan KM, Kibuule D, Banerjee R, McIntyre E, et al. (2007) Quantitative diffusion tensor imaging detects dopaminergic neuronal degeneration in a murine model of Parkinson's disease. Neurobiol Dis 26: 590-596.
66. Chan LL, Rumpel H, Yap K, Lee E, Loo HV, et al. (2007) Case control study of diffusion tensor imaging in Parkinson's disease. J Neurol Neurosurg Psychiatry 78: 1383-1386.
67. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5: 143-156.
68. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, et al. (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31: 1487-1505.
69. Tuch DS, Salat DH, Wisco JJ, Zaleta AK, Hevelone ND, et al. (2005) Choice reaction time performance correlates with diffusion anisotropy in white matter pathways supporting visuospatial attention. Proc Natl Acad Sci U S A 102: 12212-12217.
70. Aharon I, Etcoff N, Ariely D, Chabris CF, O'Connor E, et al. (2001) Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 32: 537-551.
71. Makris N, Gasic GP, Kennedy DN, Hodge SM, Kaiser JR, et al. (2008) Cortical thickness abnormalities in cocaine addiction-a reflection of both drug use and a pre-existing disposition to drug abuse? Neuron 60: 174-188.
72. Wainer H (1978) Gapping. Psychometrika 43: 203-212.
73. Fava M, Rush AJ, Alpert JE, Balasubramani GK, Wisniewski SR, et al. (2008) Difference in treatment outcome in outpatients with anxious versus nonanxious depression: a STAR*D report. Am J Psychiatry 165: 342-351.
74. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15: 435-455.
75. Harsan LA, Poulet P, Guignard B, Parizel N, Skoff RP, et al. (2007) Astrocytic hypertrophy in dysmyelination influences the diffusion anisotropy of white matter. J Neurosci Res 85: 935-944.
76. Jansen JF, Lemmens EM, Strijkers GJ, Prompers JJ, Schijns OE, et al. (2008) Short- and long-term limbic abnormalities after experimental febrile seizures. Neurobiol Dis.
77. Ongur D, Drevets WC, Price JL (1998) Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 95: 13290-13295.
78. Ballmaier M, Toga AW, Blanton RE, Sowell ER, Lavretsky H, et al. (2004) Anterior cingulate, gyrus rectus, and orbitofrontal abnormalities in elderly depressed patients: an MRI-based parcellation of the prefrontal cortex. Am J Psychiatry 161: 99-108.
79. Botteron KN, Raichle ME, Drevets WC, Heath AC, Todd RD (2002) Volumetric reduction in left subgenual prefrontal cortex in early onset depression. Biol Psychiatry 51: 342-344.
80. Bains JS, Oliet SH (2007) Glia: they make your memories stick! Trends Neurosci. M.
81. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291: 657-661.
82. Russo SJ, Bolanos CA, Theobald DE, DeCarolis NA, Renthal W, et al. (2007) IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat Neurosci 10: 93-99.
83. Haber SN, Fudge JL, McFarland NR (2000) Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20: 2369-2382.
84. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275: 1593-1599.
85. Nobre MJ, Lopes MG, Brandao ML (2004) Defense reaction mediated by NMDA mechanisms in the inferior colliculus is modulated by GABAergic nigrocollicular pathways. Brain Res 999: 124-131.
86. Wiedemann G, Pauli P, Dengler W (2001) A priori expectancy bias in patients with panic disorder. J Anxiety Disord 15: 401-412.
87. Compton RJ, Carp J, Chaddock L, Fineman SL, Quandt LC, et al. (2007) Anxiety and error monitoring: Increased error sensitivity or altered expectations? Brain Cogn.
88. Chan CK, Lovibond PF (1996) Expectancy bias in trait anxiety. J Abnorm Psychol 105: 637-647.
89. Wise RA (2009) Roles for nigrostriatal-not just mesocorticolimbic-dopamine in reward and addiction. Trends Neurosci 32: 517-524.
90. Blood AJ (2008) New hypotheses about postural control support the notion that all dystonias are manifestations of excessive brain postural function. Biosci Hypotheses 1: 14-25.
91. Guiard BP, El Mansari M, Blier P (2009) Prospect of a Dopamine Contribution in the Next Generation of Antidepressant Drugs: The Triple Reuptake Inhibitors. Curr Drug Targets.
92. Guimaraes AR, Melcher JR, Talavage TM, Baker JR, Ledden P, et al. (1998) Imaging subcortical auditory activity in humans. Hum Brain Mapp 6: 33-41.
93. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20: 9104-9110.
94. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, et al. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805-809.
95. Blood AJ, Tuch DS, Makris N, Makhlouf ML, Sudarsky LR, et al. (2006) White matter abnormalities in dystonia normalize after botulinum toxin treatment. Neuroreport 17: 1251-1255.