Magnetic resonance imaging in late-life depression: Multimodal examination of network disruption

Archives of General Psychiatry

Volumn 69, Issue 7, 2012, Pages 680-689

  Sexton, Claire E ^a   Allan, Charlotte L ^a   Le Masurier, Marisa ^b   McDermott, Lisa M ^c   Kalu, Ukwuori G ^a   Herrmann, Lucie L ^d   Mäurer, Matthias ^e   Bradley, Kevin M ^f   Mackay, Clare E ^a   Ebmeier, Klaus P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Westmorland General Hospital   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d NHS GREATER GLASGOW AND CLYDE   (United Kingdom)

^e FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^f OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; CASE CONTROL STUDY; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; FRACTIONAL ANISOTROPY; GRAY MATTER; HUMAN; LATE LIFE DEPRESSION; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; VOXEL BASED MORPHOMETRY; WHITE MATTER;

AGED; AGED, 80 AND OVER; BRAIN; BRAIN MAPPING; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; DEPRESSIVE DISORDER; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED;

EID: 84863558346     PISSN: 0003990X     EISSN: 15383636     Source Type: Journal    
DOI: 10.1001/archgenpsychiatry.2011.1862     Document Type: Article

References (80)

1. Beekman AT, Copeland JR, Prince MJ. Review of community prevalence of depression in later life. Br J Psychiatry. 1999;174:307-311. (Pubitemid 29179713)
2. Copeland JR, Beekman AT, Dewey ME, Hooijer C, Jordan A, Lawlor BA, Lobo A, Magnusson H, Mann AH, Meller I, Prince MJ, Reischies F, Turrina C, deVries MW, Wilson KC. Depression in Europe: geographical distribution among older people. Br J Psychiatry. 1999;174:312-321. (Pubitemid 29179714)
3. Steffens DC, Fisher GG, Langa KM, Potter GG, Plassman BL. Prevalence of depression among older Americans: the Aging, Demographics and Memory Study. Int Psychogeriatr. 2009;21(5):879-888.
4. Christensen K, Doblhammer G, Rau R, Vaupel JW. Ageing populations: the challenges ahead. Lancet. 2009;374(9696):1196-1208.
5. Alexopoulos GS. Frontostriatal and limbic dysfunction in late-life depression. Am J Geriatr Psychiatry. 2002;10(6):687-695. (Pubitemid 35315704)
6. Koolschijn PCMP, van Haren NEM, Lensvelt-Mulders GJLM, Hulshoff Pol HE, Kahn RS. Brain volume abnormalities in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Hum Brain Mapp. 2009;30 (11):3719-3735.
7. Sexton CE, Mackay CE, Ebmeier KP. A systematic review of diffusion tensor imaging studies in affective disorders. Biol Psychiatry. 2009;66(9):814-823.
8. Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, Kenna H, Reiss AL, Schatzberg AF. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry. 2007;62(5):429-437. (Pubitemid 47284017)
9. Hamilton JP, Chen G, Thomason ME, Schwartz ME, Gotlib IH. Investigating neural primacy in major depressive disorder: multivariate Granger causality analysis of resting- state fMRI time-series data. Mol Psychiatry. 2011;16(7):763-772.
10. Sheline YI, Price JL, Yan Z, Mintun MA. Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proc Natl Acad Sci U S A. 2010;107(24):11020-11025.
11. Zhou Y, Yu C, Zheng H, Liu Y, Song M, Qin W, Li K, Jiang T. Increased neural resources recruitment in the intrinsic organization in major depression. J Affect Disord. 2010;121(3):220-230.
12. Burzynska AZ, Preuschhof C, Bäckman L, Nyberg L, Li SC, Lindenberger U, Heekeren HR. Age-related differences in white matter microstructure: region-specific patterns of diffusivity. Neuroimage. 2010;49(3):2104-2112.
13. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003;20(3):1714-1722. (Pubitemid 37468277)
14. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002;17(3):1429-1436. (Pubitemid 35333862)
15. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage. 2005;26(1):132-140. (Pubitemid 40602893)
16. Sun SW, Liang HF, Trinkaus K, Cross AH, Armstrong RC, Song SK. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med. 2006;55(2):302-308. (Pubitemid 43238098)
17. Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix LR, Virta A, Basser P. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage. 2001;13(6, pt 1):1174-1185. (Pubitemid 32553548)
18. Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL. Disruption of large-scale brain systems in advanced aging. Neuron. 2007; 56(5):924-935. (Pubitemid 350181355)
19. Herrmann LL, Le Masurier M, Ebmeier KP. White matter hyperintensities in late life depression: a systematic review. J Neurol Neurosurg Psychiatry. 2008; 79(6):619-624. (Pubitemid 351829430)
20. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-Patient Edition. New York: Biometrics Research, New York State Psychiatric Institute; 2007.
21. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state": a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975; 12(3):189-198.
22. Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR. The Addenbrooke's Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry. 2006;21(11):1078-1085. (Pubitemid 44762726)
23. McGurn B, Starr JM, Topfer JA, Pattie A, Whiteman MC, Lemmon HA, Whalley LJ, Deary IJ. Pronunciation of irregular words is preserved in dementia, validating premorbid IQ estimation. Neurology. 2004;62(7):1184-1186. (Pubitemid 38456515)
24. Briggs GG, Nebes RD. Patterns of hand preference in a student population. Cortex. 1975;11(3):230-238.
25. D'Agostino RB, Wolf PA, Belanger AJ, KannelWB.Stroke risk profile: adjustment for antihypertensive medication. The Framingham Study. Stroke. 1994;25(1):40-43.
26. Hamilton M. Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol. 1967;6(4):278-296.
27. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO. Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res. 1982-1983;17(1):37-49. (Pubitemid 13123113)
28. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen- Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23(suppl 1):S208-S219.
29. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17(3): 143-155. (Pubitemid 35253488)
30. Zhang Y, Brady M, Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging. 2001;20(1):45-57. (Pubitemid 32293419)
31. Patenaude B, Smith SM, Kennedy DN, Jenkinson M. A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage. 2011;56(3): 907-922.
32. Ashburner J, Friston KJ. Voxel-based morphometry - the methods. Neuroimage. 2000;11(6, pt 1):805-821. (Pubitemid 30437668)
33. Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston KJ, Frackowiak RSJ. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001;14(1, pt 1):21-36. (Pubitemid 32552740)
34. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17(2):825-841. (Pubitemid 35317016)
35. Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal. 2001;5(2):143-156. (Pubitemid 35282800)
36. Andersson JLR, Jenkinson M, Smith S. Non-linear optimisation. FMRIB technical report TR07JA1. http://www.fmrib.ox.ac.uk/analysis/techrep. Published 2007. Accessed April 6, 2012.
37. Andersson JLR, Jenkinson M, Smith S. Non-linear registration, aka spatial normalisation. FMRIB technical report TR07JA2. http://www.fmrib.ox.ac.uk /analysis/techrep. Accessed May 3, 2012.
38. Rueckert D, Sonoda LI, Hayes C, Hill DL, Leach MO, Hawkes DJ. Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging. 1999;18(8):712-721. (Pubitemid 32262025)
39. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. 2002;15(1):1-25. (Pubitemid 34020610)
40. Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2009;44(1):83-98.
41. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TEJ. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006; 31(4):1487-1505.
42. Mori S, Wakana S, Nagae-Poetscher LM, van Zijl PCM. MRI Atlas of Human White Matter. Amsterdam, the Netherlands: Elsevier BV; 2005.
43. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351-356. (Pubitemid 17104996)
44. Beckmann CF, Smith SM. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging. 2004;23(2): 137-152.
45. Damoiseaux JS, Rombouts SARB, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A. 2006;103(37):13848-13853. (Pubitemid 44413996)
46. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE. Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci U S A. 2009;106(17): 7209-7214.
47. Williams SS, Williams J, Combrinck M, Christie S, Smith AD, McShane R. Olfactory impairment is more marked in patients with mild dementia with Lewy bodies than those with mild Alzheimer disease. J Neurol Neurosurg Psychiatry. 2009;80(6):667-670.
48. Hyvärinen A. Fast and robust fixed-point algorithms for independent component analysis. IEEE Trans Neural Netw. 1999;10(3):626-634.
49. Beckmann CF, DeLuca M, Devlin JT, Smith SM. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci. 2005;360(1457):1001-1013. (Pubitemid 41672861)
50. Ashtari M, Greenwald BS, Kramer-Ginsberg E, Hu J, Wu H, Patel M, Aupperle P, Pollack S. Hippocampal/amygdala volumes in geriatric depression. Psychol Med. 1999;29(3):629-638. (Pubitemid 29261351)
51. Avila R, Ribeiz S, Duran FL, Arrais JP, Moscoso MA, Bezerra DM, Jaluul O, Castro CC, Busatto GF, Bottino CM. Effect of temporal lobe structure volume on memory in elderly depressed patients. Neurobiol Aging. 2011;32(10):1857-1867.
52. Janssen J, Hulshoff Pol HE, de Leeuw FE, Schnack HG, Lampe IK, Kok RM, Kahn RS, Heeren TJ. Hippocampal volume and subcortical white matter lesions in late life depression: comparison of early and late onset depression. J Neurol Neurosurg Psychiatry. 2007;78(6):638-640. (Pubitemid 46853904)
53. O'Brien JT, Lloyd A, McKeith I, Gholkar A, Ferrier N. A longitudinal study of hippocampal volume, cortisol levels, and cognition in older depressed subjects. Am J Psychiatry. 2004;161(11):2081-2090. (Pubitemid 39441410)
54. Taylor WD, Steffens DC, Payne ME, MacFall JR, Marchuk DA, Svenson IK, Krishnan KR. Influence of serotonin transporter promoter region polymorphisms on hippocampal volumes in late-life depression. Arch Gen Psychiatry. 2005;62(5): 537-544. (Pubitemid 40628883)
55. Weber K, Giannakopoulos P, Delaloye C, de Bilbao F, Moy G, Moussa A, Rubio MM, Ebbing K, Meuli R, Lazeyras F, Meiler-Mititelu C, Herrmann FR, Gold G, Canuto A. Volumetric MRI changes, cognition and personality traits in old age depression. J Affect Disord. 2010;124(3):275-282.
56. Zhao Z, Taylor WD, Styner M, Steffens DC, Krishnan KR, MacFall JR. Hippocampus shape analysis and late-life depression. PLoS One. 2008;3(3):e1837. doi: 10.1371/journal.pone.0001837.
57. Koolschijn PC, van Haren NE, Schnack HG, Janssen J, Hulshoff Pol HE, Kahn RS. Cortical thickness and voxel-based morphometry in depressed elderly. Eur Neuropsychopharmacol. 2010;20(6):398-404.
58. Shimony JS, Sheline YI, D'Angelo G, Epstein AA, Benzinger TL, Mintun MA, McKinstry RC, Snyder AZ. Diffuse microstructural abnormalities of normal-appearing white matter in late life depression: a diffusion tensor imaging study. Biol Psychiatry. 2009;66(3):245-252.
59. Hamidi M, Drevets WC, Price JL. Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol Psychiatry. 2004;55(6):563-569. (Pubitemid 38315029)
60. Uranova NA, Vostrikov VM, Orlovskaya DD, Rachmanova VI. Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophr Res. 2004;67(2-3): 269-275. (Pubitemid 38251458)
61. Regenold WT, Phatak P, Marano CM, Gearhart L, Viens CH, Hisley KC. Myelin staining of deep white matter in the dorsolateral prefrontal cortex in schizophrenia, bipolar disorder, and unipolar major depression. Psychiatry Res. 2007; 151(3):179-188. (Pubitemid 46829420)
62. Aston C, Jiang L, Sokolov BP. Transcriptional profiling reveals evidence for signaling and oligodendroglial abnormalities in the temporal cortex from patients with major depressive disorder. Mol Psychiatry. 2005;10(3):309-322. (Pubitemid 40432684)
63. Rainer MK, Mucke HA, Zehetmayer S, Krampla W, Kuselbauer T, Weissgram S, Jungwirth S, Tragl KH, Fischer P. Data from the VITA Study do not support the concept of vascular depression. Am J Geriatr Psychiatry. 2006;14(6):531-537. (Pubitemid 43849531)
64. Sheline YI, Price JL, Vaishnavi SN, Mintun MA, Barch DM, Epstein AA, Wilkins CH, Snyder AZ, Couture L, Schechtman K, McKinstry RC. Regional white matter hyperintensity burden in automated segmentation distinguishes late-life depressed subjects from comparison subjects matched for vascular risk factors. Am J Psychiatry. 2008;165(4):524-532. (Pubitemid 351694296)
65. Thomas AJ, O'Brien JT, Davis S, Ballard C, Barber R, Kalaria RN, Perry RH. Ischemic basis for deep white matter hyperintensities in major depression: a neuropathological study. Arch Gen Psychiatry. 2002;59(9):785-792. (Pubitemid 35001143)
66. Craddock RC, Holtzheimer PE III, Hu XP, Mayberg HS. Disease state prediction from resting state functional connectivity. Magn Reson Med. 2009;62(6):1619-1628.
67. Veer IM, Beckmann CF, van Tol M-J, Ferrarini L, Milles J, Veltman DJ, Aleman A, van Buchem MA, van der Wee NJ, Rombouts SA. Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Front Syst Neurosci. 2010;4:41.
68. Jones DK. The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med. 2004;51(4): 807-815. (Pubitemid 38420459)
69. Kempton MJ, Salvador Z, Munafò MR, Geddes JR, Simmons A, Frangou S, Williams SCR. Structural neuroimaging studies in major depressive disorder: metaanalysis and comparison with bipolar disorder. Arch Gen Psychiatry. 2011; 68(7):675-690.
70. Egger K, Schocke M, Weiss E, Auffinger S, Esterhammer R, Goebel G, Walch T, Mechtcheriakov S, Marksteiner J. Pattern of brain atrophy in elderly patients with depression revealed by voxel-based morphometry. Psychiatry Res. 2008;164 (3):237-244.
71. Bell-McGinty S, Butters MA, Meltzer CC, Greer PJ, Reynolds CF III, Becker JT. Brain morphometric abnormalities in geriatric depression: long-term neurobiological effects of illness duration. Am J Psychiatry. 2002;159(8):1424-1427. (Pubitemid 34832728)
72. Janssen J, Hulshoff Pol HE, Lampe IK, Schnack HG, de Leeuw FE, Kahn RS, Heeren TJ. Hippocampal changes and white matter lesions in early-onset depression. Biol Psychiatry. 2004;56(11):825-831. (Pubitemid 39575455)
73. Lai T, Payne ME, Byrum CE, Steffens DC, Krishnan KR. Reduction of orbital frontal cortex volume in geriatric depression. Biol Psychiatry. 2000;48(10):971-975.
74. Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL. Functional-anatomic fractionation of the brain's default network. Neuron. 2010;65(4): 550-562.
75. Sheline YI, Barch DM, Price JL, Rundle MM, Vaishnavi SN, Snyder AZ, Mintun MA, Wang S, Coalson RS, Raichle ME. The default mode network and selfreferential processes in depression. Proc Natl Acad Sci U S A. 2009;106(6): 1942-1947.
76. Bluhm R, Williamson P, Lanius R, Théberge J, Densmore M, Bartha R, Neufeld R, Osuch E. Resting state default-mode network connectivity in early depression using a seed region-of-interest analysis: decreased connectivity with caudate nucleus. Psychiatry Clin Neurosci. 2009;63(6):754-761.
77. Cullen KR, Gee DG, Klimes-Dougan B, Gabbay V, Hulvershorn L, Mueller BA, Camchong J, Bell CJ, Houri A, Kumra S, Lim KO, Castellanos FX, Milham MP. A preliminary study of functional connectivity in comorbid adolescent depression. Neurosci Lett. 2009;460(3):227-231.
78. Versace A, Almeida JR, Quevedo K, Thompson WK, Terwilliger RA, Hassel S, Kupfer DJ, Phillips ML. Right orbitofrontal corticolimbic and left corticocortical white matter connectivity differentiate bipolar and unipolar depression. Biol Psychiatry. 2010;68(6):560-567.
79. Groves AR, Beckmann CF, Smith SM, Woolrich MW. Linked independent component analysis for multimodal data fusion. Neuroimage. 2011;54(3):2198- 2217.
80. Chanraud S, Zahr N, Sullivan EV, Pfefferbaum A. MR diffusion tensor imaging: a window into white matter integrity of the working brain. Neuropsychol Rev. 2010; 20(2):209-225.