Illness progression, recent stress, and morphometry of hippocampal subfields and medial prefrontal cortex in major depression

Biological Psychiatry

Volumn 77, Issue 3, 2015, Pages 285-294

  Treadway, Michael T ^a   Waskom, Michael L ^b   Dillon, Daniel G ^a   Holmes, Avram J ^c,d   Park, Min Tae M ^e   Chakravarty, M Mallar ^e,f   Dutra, Sunny J ^d   Polli, Frida E ^g   Iosifescu, Dan V ^h   Fava, Maurizio ^a   Gabrieli, John D E ^g   Pizzagalli, Diego A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b STANFORD UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d YALE UNIVERSITY   (United States)

^e CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

^g MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^h MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Dentate gyrus; Hippocampus; MAGeT brain; Major depression; mPFC; MRI

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BECK DEPRESSION INVENTORY; CONTROLLED STUDY; DENTATE GYRUS; DISEASE COURSE; FEMALE; HIPPOCAMPUS; HUMAN; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; MIDDLE FRONTAL GYRUS; MORPHOMETRICS; NUCLEAR MAGNETIC RESONANCE IMAGING; PARAHIPPOCAMPAL GYRUS; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; STRATUM LACUNOSUM MOLECULARE; STRATUM RADIATUM; STRESS; MENTAL STRESS; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; RECURRENT DISEASE;

ADULT; AMYGDALA; DEPRESSIVE DISORDER, MAJOR; DISEASE PROGRESSION; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; ORGAN SIZE; PREFRONTAL CORTEX; RECURRENCE; STRESS, PSYCHOLOGICAL;

EID: 84925718653     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.06.018     Document Type: Article

References (78)

1. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE (2005): Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62:617-627.
2. Kessler RC (2012): The costs of depression. Psychiatr Clin North Am 35:1-14.
3. Ferrari AJ, Charlson FJ, Norman RE, Patten SB, Freedman G, Murray CJ, et al. (2013): Burden of depressive disorders by country, sex, age, and year: Findings from the global burden of disease study 2010. PLoS Med 10:e1001547.
4. APA (2000): Practice guideline for the treatment of patients with major depressive disorder (revision). Am J Psychiatry 157:1-45.
5. Monroe SM, Harkness KL (2011): Recurrence in major depression: A conceptual analysis. Psychol Rev 118:655-674.
6. Monroe SM, Harkness KL (2005): Life stress, the "kindling " hypothesis, and the recurrence of depression: Considerations from a life stress perspective. Psychol Rev 112:417-445.
7. Post RM (1992): Transduction of psychosocial stress into the neurobiology. Am J Psychiatry 149:999-1010.
8. Farmer A, Harris T, Redman K, Sadler S, Mahmood A, McGuffin P (2000): Cardiff Depression Study: A sib-pair study of life events and familiality in major depression. Br J Psychiatry 176:150-155.
9. Stroud CB, Davila J, Hammen C, Vrshek-Schallhorn S (2011): Severe and nonsevere events in first onsets versus recurrences of depression: Evidence for stress sensitization. J Abnorm Psychol 120:142.
10. Ormel J, Oldehinkel AJ, Brilman EI (2001): The interplay and etiological continuity of neuroticism, difficulties, and life events in the etiology of major and subsyndromal, first and recurrent depressive episodes in later life. Am J Psychiatry 158:885-891.
11. McEwen BS (2007): Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 87:873-904.
12. Sorrells SF, Sapolsky RM (2007): An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 21:259-272.
13. Sapolsky RM (2000): Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57:925-935.
14. Kempton MJ, Salvador Z, Munafo MR, Geddes JR, Simmons A, Frangou S, et al. (2011): Structural neuroimaging studies in major depressive disorder. Meta-analysis and comparison with bipolar disorder. Arch Gen Psychiatry 68:675-690.
15. Koolschijn PC, van Haren NE, Lensvelt-Mulders GJ, Hulshoff Pol HE, Kahn RS (2009): Brain volume abnormalities in major depressive disorder: A meta-analysis of magnetic resonance imaging studies. Hum Brain Mapp 30:3719-3735.
16. Bora E, Fornito A, Yucel M, Pantelis C (2010): Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder. Biol Psychiatry 67:1097-1105.
17. Bora E, Harrison BJ, Davey CG, Yucel M, Pantelis C (2011): Meta-analysis of volumetric abnormalities in cortico-striatal-pallidal-thalamic circuits in major depressive disorder. Psychol Med 42:671-681.
18. Chana G, Landau S, Beasley C, Everall IP, Cotter D (2003): Two-dimensional assessment of cytoarchitecture in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia: Evidence for decreased neuronal somal size and increased neuronal density. Biol Psychiatry 53:1086-1098.
19. Cotter D, Mackay D, Landau S, Kerwin R, Everall I (2001): Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 58:545-553.
20. Monkul E, Hatch JP, Nicoletti MA, Spence S, Brambilla P, Lacerda AL, et al. (2006): Fronto-limbic brain structures in suicidal and non-suicidal female patients with major depressive disorder. Mol Psychiatry 12:360-366.
21. Sheline YI, Sanghavi M, Mintun MA, Gado MH (1999): Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 19:5034-5043.
22. MacQueen GM, Campbell S, McEwen BS, Macdonald K, Amano S, Joffe RT, et al. (2003): Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci U S A 100:1387-1392.
23. Frodl T, Jager M, Smajstrlova I, Born C, Bottlender R, Palladino T, et al. (2008): Effect of hippocampal and amygdala volumes on clinical outcomes in major depression: A 3-year prospective magnetic resonance imaging study. J Psychiatry Neurosci 33:423-430.
24. Holmes AJ, Lee PH, Hollinshead MO, Bakst L, Roffman JL, Smoller JW, et al. (2012): Individual differences in amygdala-medial prefrontal anatomy link negative affect, impaired social functioning, and polygenic depression risk. J Neurosci 32:18087-18100.
25. Arnone D, McKie S, Elliott R, Juhasz G, Thomas EJ, Downey D, et al. (2013): State-dependent changes in hippocampal grey matter in depression. Mol Psychiatry 18:1265-1272.
26. MacQueen G, Frodl T (2010): The hippocampus in major depression: Evidence for the convergence of the bench and bedside in psychiatric research? Mol Psychiatry 16:252-264.
27. Yucel K, McKinnon MC, Chahal R, Taylor VH, Macdonald K, Joffe R, et al. (2008): Anterior cingulate volumes in never-treated patients with major depressive disorder. Neuropsychopharmacology 33:3157-3163.
28. Plomin R, Haworth CM, Davis OS (2009): Common disorders are quantitative traits. Nat Rev Genet 10:872-878.
29. Pizzagalli DA, Treadway MT (2014): Neuroimaging approaches to the study of major depressive disorder - from regions to circuits. In: Gotlib IH, Hammen C, editors. Handbook of Depression, 3rd ed. New York: Guilford Press.
30. Winterburn JL, Pruessner JC, Chavez S, Schira MM, Lobaugh NJ, Voineskos AN, et al. (2013): A novel in vivo atlas of human hippocampal subfields using high-resolution 3T magnetic resonance imaging. Neuroimage 74:254-265.
31. Pipitone J, Park MT, Winterburn J, Lett TA, Lerch JP, Pruessner JC, et al. (2014): Multi-atlas segmentation of the whole hippocampus and subfields using multiple automatically generated templates [published online ahead of print April 29]. Neuroimage.
32. Hamilton JP, Siemer M, Gotlib IH (2008): Amygdala volume in major depressive disorder: A meta-analysis of magnetic resonance imaging studies. Mol Psychiatry 13:993-1000.
33. Grieve SM, Clark CR, Williams LM, Peduto AJ, Gordon E (2005): Preservation of limbic and paralimbic structures in aging. Hum Brain Mapp 25:391-401.
34. First M, Spitzer R, Gibbon M, Williams J (2002): Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition.(SCID-I/P). New York: Biometrics Research, New York State Psychiatric Institute.
35. Hamilton M (1960): A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56-62.
36. Cohen S, Kamarck T, Mermelstein R (1983): A global measure of perceived stress. J Health Soc Behav 24:385-396.
37. Chakravarty MM, Steadman P, Eede MC, Calcott RD, Gu V, Shaw P, et al. (2013): Performing label-fusion-based segmentation using multiple automatically generated templates. Hum Brain Mapp 34:2635-2654.
38. Collins DL, Pruessner JC (2010): Towards accurate, automatic segmentation of the hippocampus and amygdala from MRI by augmenting ANIMAL with a template library and label fusion. Neuroimage 52:1355-1366.
39. Heckemann RA, Keihaninejad S, Aljabar P, Rueckert D, Hajnal JV, Hammers A (2010): Improving intersubject image registration using tissue-class information benefits robustness and accuracy of multiatlas based anatomical segmentation. Neuroimage 51:221-227.
40. Aljabar P, Heckemann RA, Hammers A, Hajnal JV, Rueckert D (2009): Multi-atlas based segmentation of brain images: Atlas selection and its effect on accuracy. Neuroimage 46:726-738.
41. Chakravarty MM, Bertrand G, Hodge CP, Sadikot AF, Collins DL (2006): The creation of a brain atlas for image guided neurosurgery using serial histological data. Neuroimage 30:359-376.
42. Entis JJ, Doerga P, Barrett LF, Dickerson BC (2012): A reliable protocol for the manual segmentation of the human amygdala and its subregions using ultra-high resolution MRI. Neuroimage 60:1226-1235.
43. Dale AM, Fischl B, Sereno MI (1999): Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179-194.
44. Fischl B, Dale AM (2000): Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 97:11050-11055.
45. Fischl B, Sereno MI, Tootell RB, Dale AM (1999): High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272-284.
46. Hagler DJ Jr, Saygin AP, Sereno MI (2006): Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. Neuroimage 33:1093-1103.
47. Chrousos GP, Gold PW (1998): A healthy body in a healthy mind - and vice versa - the damaging power of "uncontrollable" stress. J Clin Endocrinol Metab 83:1842-1845.
48. Radley JJ, Sawchenko PE (2011): A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J Neurosci 31:9683-9695.
49. Radley JJ, Rocher AB, Miller M, Janssen WG, Liston C, Hof PR, et al. (2006): Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 16:313-320.
50. Cook SC, Wellman CL (2004): Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60:236-248.
51. Cerqueira JJ, Pego JM, Taipa R, Bessa JM, Almeida OF, Sousa N (2005): Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 25:7792-7800.
52. McEwen BS (1999): Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
53. Dias-Ferreira E, Sousa JC, Melo I, Morgado P, Mesquita AR, Cerqueira JJ, et al. (2009): Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325:621-625.
54. Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007): The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 27:2781-2787.
55. Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, et al. (2006): Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26:7870-7874.
56. Soares JM, Sampaio A, Ferreira LM, Santos NC, Marques F, Palha JA, et al. (2012): Stress-induced changes in human decision-making are reversible. Transl Psychiatry 2:e131.
57. Castro-Fornieles J, Bargallo N, Lazaro L, Andres S, Falcon C, Plana MT, et al. (2009): A cross-sectional and follow-up voxel-based morphometric MRI study in adolescent anorexia nervosa. J Psychiatr Res 43:331-340.
58. Treadway MT, Grant MM, Ding Z, Hollon SD, Gore JC, Shelton RC (2009): Early adverse events, HPA activity and rostral anterior cingulate volume in MDD. PLoS One 4:e4887.
59. Drevets WC, Price JL, Simpson JR, Todd RD, Reich T, Vannier M, et al. (1997): Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824-827.
60. Deschwanden A, Karolewicz B, Feyissa AM, Treyer V, Ametamey SM, Johayem A, et al. (2011): Reduced metabotropic glutamate receptor 5 density in major depression determined by [11C]ABP688 PET and postmortem study. Am J Psychiatry 168:727-734.
61. Schermuly I, Wolf D, Lieb K, Stoeter P, Fellgiebel A (2011): State dependent posterior hippocampal volume increases in patients with major depressive disorder. J Affect Disord 135:405-409.
62. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn A-M, Nordborg C, Peterson DA, et al. (1998): Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
63. Monje ML, Toda H, Palmer TD (2003): Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760-1765.
64. Burt DB, Zembar MJ, Niederehe G (1995): Depression and memory impairment: A meta-analysis of the association, its pattern, and specificity. Psychol Bull 117:285.
65. Bremner JD, Vythilingam M, Vermetten E, Vaccarino V, Charney DS (2004): Deficits in hippocampal and anterior cingulate functioning during verbal declarative memory encoding in midlife major depression. Am J Psychiatry 161:637-645.
66. Gorwood P, Corruble E, Falissard B, Goodwin G (2008): Toxic effects of depression on brain function: Impairment of delayed recall and the cumulative length of depressive disorder in a large sample of depressed outpatients. Am J Psychiatry 165:731-739.
67. Engvig A, Fjell AM, Westlye LT, Skaane NV, Sundseth O, Walhovd KB (2012): Hippocampal sub fi eld volumes correlate with memory training benefi t in subjective memory impairment. Neuroimage 61:188-194.
68. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005): Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365-371.
69. Amat J, Paul E, Watkins LR, Maier SF (2008): Activation of the ventral medial prefrontal cortex during an uncontrollable stressor reproduces both the immediate and long-term protective effects of behavioral control. Neuroscience 154:1178-1186.
70. Maier SF, Watkins LR (2010): Role of the medial prefrontal cortex in coping and resilience. Brain Res 1355:52-60.
71. Dillon DG, Pizzagalli DA (2013): Evidence of successful modulation of brain activation and subjective experience during reappraisal of negative emotion in unmedicated depression. Psychiatry Res 212:99-107.
72. Diener C, Kuehner C, Brusniak W, Ubl B, Wessa M, Flor H (2012): A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. Neuroimage 61:677-685.
73. Ochsner KN, Gross JJ (2005): The cognitive control of emotion. Trends Cogn Sci 9:242-249.
74. Mak AK, Wong M, Han S-H, Lee T (2009): Gray matter reduction associated with emotion regulation in female outpatients with major depressive disorder: A voxel-based morphometry study. Prog Neuropsychopharmacol Biol Psychiatry 33:1184-1190.
75. Abe O, Yamasue H, Kasai K, Yamada H, Aoki S, Inoue H, et al. (2010): Voxel-based analyses of gray/white matter volume and diffusion tensor data in major depression. Psychiatry Res 181:64-70.
76. Davidson RJ (2004): What does the prefrontal cortex " do" in affect: Perspectives on frontal EEG asymmetry research. Biol Psychol 67:219-234.
77. Nusslock R, Shackman AJ, Harmon-Jones E, Alloy LB, Coan JA, Abramson LY (2011): Cognitive vulnerability and frontal brain asymmetry: Common predictors of first prospective depressive episode. J Abnormal 120:497-503.
78. Harmon-Jones E, Gable PA, Peterson CK (2010): The role of asymmetric frontal cortical activity in emotion-related phenomena: A review and update. Biol Psychology 84:451-462.