Differential relationships between apathy and depression with white matter microstructural changes and functional outcomes

Brain

Volumn 138, Issue 12, 2015, Pages 3803-3815

  Hollocks, Matthew J ^a   Lawrence, Andrew J ^a   Brookes, Rebecca L ^a   Barrick, Thomas R ^b   Morris, Robin G ^c   Husain, Masud ^d   Markus, Hugh S ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

diffusion tensor imaging; emotion; lacunar stroke; motivation; vascular dementia

Indexed keywords

ADULT; AGED; APATHY; ARTICLE; CEREBROVASCULAR DISEASE; CINGULUM (BRAIN); COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; EMOTIONALITY; EXECUTIVE FUNCTION; FEMALE; FRACTIONAL ANISOTROPY; FUNCTIONAL STATUS; GERIATRIC DEPRESSION SCALE; HUMAN; LACUNAR STROKE; LEUKOARAIOSIS; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; QUALITY OF LIFE; SYMPTOM; UNCINATE FASCICULUS; WHITE MATTER LESION; ANISOTROPY; BRAIN; COMPLICATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOLOGY; WHITE MATTER;

AGED; ANISOTROPY; APATHY; BRAIN; CEREBRAL SMALL VESSEL DISEASES; COGNITION DISORDERS; DEPRESSION; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; NEUROIMAGING; QUALITY OF LIFE; WHITE MATTER;

EID: 84951008083     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv304     Document Type: Article

References (80)

1. Adam R, Leff A, Sinha N, Turner C, Bays P, Draganski B, et al. Dopamine reverses reward insensitivity in apathy following globus pallidus lesions. Cortex 2013; 49: 1292-303.
2. Adams KB, Matto HC, Sanders S. Confirmatory factor analysis of the geriatric depression scale. Gerontologist 2004; 44: 818-26.
3. Agosta F, Galantucci S, Svetel M, LukićMJ, Copetti M, Davidovic K, et al. Clinical, cognitive, and behavioural correlates of white matter damage in progressive supranuclear palsy. J Neurol 2014; 261: 913-24.
4. Alexopoulos GS, Hoptman MJ, Yuen G, Kanellopoulos DK, Seirup J, Lim KO, et al. Functional connectivity in apathy of late-life depression: a preliminary study. J Affect Disord 2013; 149: 398-405.
5. Apostolova LG, Akopyan GG, Partiali N, Steiner CA, Dutton RA, Hayashi KM, et al. Structural correlates of apathy in Alzheimers disease. Dement Geriatr Cogn Disord 2007; 24: 91-7.
6. Ashburner J, Friston KJ. Voxel-based morphometry-the methods. Neuroimage 2000; 11: 805-21.
7. Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 2011; 54: 2033-44.
8. Basser PJ, Mattiello J, LeBihan D. Estimation of the effective selfdiffusion tensor from the NMR spin echo. J Magn Reson B 1994; 103: 247-54.
9. Bookstein FL. Voxel-based morphometry should not be used with imperfectly registered images. Neuroimage 2001; 14: 1454-62.
10. Brookes RL, Hannesdottir K, Lawrence R, Morris RG, Markus HS. Brief Memory and Executive Test: evaluation of a new screening test for cognitive impairment due to small vessel disease [Internet]. Age Ageing 2012; 41: 2128.
11. Brookes RL, Herbert V, Lawrence AJ, Morris RG, Markus HS. Depression in small-vessel disease relates to white matter ultrastructural damage, not disability. Neurology 2014a; 83: 1417-23.
12. Brookes RL, Herbert V, Paul S, Hannesdottir K, Markus HS, Morris RG. Executive dysfunction, awareness deficits and quality of life in patients with cerebral small vessel disease: a structural equation model. Neuropsychology 2014b; 28: 247-53.
13. Brookes RL, Hollocks MJ, Khan U, Morris RG, Markus HS. The Brief Memory and Executive Test (BMET) for detecting vascular cognitive impairment in small vessel disease: a validation study. BMC Med 2015; 13: 290.
14. Brookes RL, Willis T a, Patel B, Morris RG, Markus HS. Depressive symptoms as a predictor of quality of life in cerebral small vessel disease, acting independently of disability; a study in both sporadic small vessel disease and CADASIL. Int J Stroke 2013; 8: 510-7.
15. Cacciari C, Moraschi M, Di Paola M, Cherubini A, Orfei MD, Giove F, et al. White matter microstructure and apathy level in amnestic mild cognitive impairment. J Alzheimers Dis 2010; 20: 501-7.
16. Chaturvedi SK, Sarmukaddam SB. Prediction of outcome in depression by negative symptoms. Acta Psychiatr Scand 1986; 74: 183-6.
17. Cohen RA, Kaplan RF, Zuffante P, Moser DJ, Jenkins MA, Salloway S, et al. Alteration of intention and self-initiated action associated with bilateral anterior cingulotomy. J Neuropsychiatry Clin Neurosci 1999; 11: 444-53.
18. Fazekas F, Chawluk JB, Zimmerma A, June M. MR signal abnormalities at 1.5 T in Alzheimer s dementia and normal aging deficiency. AJR Am J Roentgenol 1987; 149: 351-6.
19. Grool AM, Geerlings MI, Sigurdsson S, Eiriksdottir G, Jonsson PV., Garcia ME, et al. Structural MRI correlates of apathy symptoms in older persons without dementia: AGES-Reykjavik Study. Neurology 2014; 82: 1628-35.
20. Grunsfeld AA, Login IS. Abulia following penetrating brain injury during endoscopic sinus surgery with disruption of the anterior cingulate circuit: case report. BMC Neurol 2006; 6: 4.
21. Hackett ML, Köhler S, OBrien JT, Mead GE. Neuropsychiatric outcomes of stroke. Lancet Neurol 2014; 13: 525-34.
22. Hahn C, Lim HK, Won WY, Ahn KJ, Jung WS, Lee CU. Apathy and white matter integrity in Alzheimers disease: a whole brain analysis with tract-based spatial statistics. PLoS One 2013; 8
23. Holroyd CB, Yeung N. Motivation of extended behaviors by anterior cingulate cortex. Trends Cogn Sci 2012; 16: 122-8.
24. HölttäEH, Laakkonen ML, Laurila J V., Strandberg TE, Tilvis RS, PitkäläKH. Apathy: prevalence, associated factors, and prognostic value among frail, older inpatients. J Am Med Dir Assoc 2012; 13: 541-5.
25. Hornberger M, Geng J, Hodges JR. Convergent grey and white matter evidence of orbitofrontal cortex changes related to disinhibition in behavioural variant frontotemporal dementia. Brain 2011; 134: 2502-12.
26. Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, et al. Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage 2008; 39: 336-47.
27. Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage 2012; 62: 782-90.
28. Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal 2001; 5: 143-56.
29. Kim G, DeCoster J, Huang C-H, Bryant AN. A meta-analysis of the factor structure of the Geriatric Depression Scale (GDS): the effects of language. Int Psychogeriatr 2012: 1-11.
30. Kim HJ, Kang SJ, Kim C, Kim GH, Jeon S, Lee JM, et al. The effects of small vessel disease and amyloid burden on neuropsychiatric symptoms: a study among patients with subcortical vascular cognitive impairments. Neurobiol Aging 2013; 34: 1913-20.
31. Kim JW, Lee DY, Choo IH, Seo EH, Kim SG, Park SY, et al. Microstructural alteration of the anterior cingulum is associated with apathy in Alzheimer disease. Am J Geriatr Psychiatry 2011; 19: 644-53.
32. Kirsch-Darrow L, Marsiske M, Okun MS, Bauer R, Bowers D. Apathy and depression: separate factors in Parkinsons disease. J Int Neuropsychol Soc 2011; 17: 1058-66.
33. Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang M-C, et al. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 2009; 46: 786-802.
34. Kohno N, Abe S, Toyoda G, Oguro H, Bokura H, Yamaguchi S. Successful treatment of post-stroke apathy by the dopamine receptor agonist ropinirole. J Clin Neurosci 2010; 17: 804-6.
35. Landes AM, Sperry SD, Strauss ME. Prevalence of apathy, dysphoria, and depression in relation to dementia severity in Alzheimers disease. J Neuropsychiatry Clin Neurosci 2005; 17: 342-9.
36. Lawrence AJ, Patel B, Morris RG, MacKinnon AD, Rich PM, Barrick TR, et al. Mechanisms of cognitive impairment in cerebral small vessel disease: multimodal MRI results from the St Georges cognition and neuroimaging in stroke (SCANS) study. PLoS One 2013; 8: e61014.
37. Levy R, Czernecki V. Apathy and the basal ganglia. J Neurol 2006; 253
38. Levy R, Dubois B. Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex 2006; 16: 916-28.
39. Makin SDJ, Turpin S, Dennis MS, Wardlaw JM. Cognitive impairment after lacunar stroke: systematic review and meta-analysis of incidence, prevalence and comparison with other stroke subtypes. J Neurol Neurosurg Psychiatry 2013; 84: 893-900.
40. Marin RS, Biedrzycki RC, Firinciogullari S. Reliability and validity of the apathy evaluation scale. Psychiatry Res 1991; 38: 143-62.
41. Marin RS, Firinciogullari S, Biedrzycki RC. The sources of convergence between measures of apathy and depression. J Affect Disord 1993; 28: 7-14.
42. Marshall GA, Monserratt L, Harwood D, Mandelkern M, Cummings JL, Sultzer DL. Positron emission tomography metabolic correlates of apathy in Alzheimer disease. Arch Neurol 2007; 64: 1015-20.
43. Martino J, Brogna C, Robles SG, Vergani F, Duffau H. Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 2010; 46: 691-9.
44. Metzler-Baddeley C, Hunt S, Jones DK, Leemans A, Aggleton JP, OSullivan MJ. Temporal association tracts and the breakdown of episodic memory in mild cognitive impairment. Neurology 2012; 79: 2233-40.
45. Mitchell AJ, Bird V, Rizzo M, Meader N. Diagnostic validity and added value of the Geriatric Depression Scale for depression in primary care: a meta-analysis of GDS30 and GDS15. J Affect Disord 2010; 125: 10-17.
46. Moretti R, Cavressi M, Tomietto P. Gait and apathy as relevant symptoms of subcortical vascular dementia. Am J Alzheimers Dis Other Demen 2015; 30: 390-9.
47. Mori S, Wakana S, Nagae-Poetscher LM, Van Zijl PCM. MRI atlas of human white matter. Amsterdam, The Netherlands: Elsevier; 2005.
48. Muthén LK, Muthén BO. Mplus users guide. Los Angeles, CA: Muthén & Muthén; 2012.
49. Neeman M, Freyer JP, Sillerud LO. A simple method for obtaining cross-term-free images for diffusion anisotropy studies in NMR microimaging. Magn Reson Med 1991; 21: 138-43.
50. OBrien JT, Firbank MJ, Krishnan MS, van Straaten ECW, van der Flier WM, Petrovic K, et al. White matter hyperintensities rather than lacunar infarcts are associated with depressive symptoms in older people: the LADIS study. Am J Geriatr Psychiatry 2006; 14: 834-41.
51. Papagno C, Miracapillo C, Casarotti A, Romero Lauro LJ, Castellano A, Falini A, et al. What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain 2011; 134: 405-14.
52. Prins ND, Van Dijk EJ, Den Heijer T, Vermeer SE, Jolles J, Koudstaal PJ, et al. Cerebral small-vessel disease and decline in information processing speed, executive function and memory. Brain 2005; 128: 2034-41.
53. Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas 1977; 1: 385-401.
54. Robert P, Onyike CU, Leentjens AFG, Dujardin K, Aalten P, Starkstein S, et al. Proposed diagnostic criteria for apathy in Alzheimers disease and other neuropsychiatric disorders. Eur Psychiatry 2009; 24: 98-104.
55. Rosenberg PB, Lanctot KL, Drye LT, Herrmann N, Scherer RW, Bachman DL, et al. Safety and efficacy of methylphenidate for apathy in Alzheimers disease: a randomized, placebo-controlled trial. J Clin Psychiatry 2013; 74: 810-6.
56. Salzman C, Wong E, Wright BC. Drug and ECT treatment of depression in the elderly, 1996-2001: a literature review. Biol Psychiatry 2002. p. 265-84.
57. Schwarz CG, Reid RI, Gunter JL, Senjem ML, Przybelski SA, Zuk SM, et al. Improved DTI registration allows voxel-based analysis that outperforms tract-based spatial statistics. Neuroimage 2014; 94: 65-78.
58. Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 2011; 12: 154-67.
59. Smith EE, Schneider JA, Wardlaw JM, Greenberg SM. Cerebral microinfarcts: the invisible lesions. Lancet Neurol 2012; 11: 272-82.
60. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp 2002; 17: 143-55.
61. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23 (Suppl 1): S208-19.
62. Sneed JR, Rindskopf D, Steffens DC, Krishnan KRR, Roose SP. The vascular depression subtype: evidence of internal validity. Biol Psychiatry 2008; 64: 491-7.
63. Sockeel P, Dujardin K, Devos D, Deneve C, Destée A, Defebvre L. The Lille apathy rating scale (LARS), a new instrument for detecting and quantifying apathy: validation in Parkinsons disease. J Neurol Neurosurg Psychiatry 2006; 77: 579-84.
64. Spalletta G, Fagioli S, Caltagirone C, Piras F. Brain microstructure of subclinical apathy phenomenology in healthy individuals. Hum Brain Mapp 2013; 34: 3193-203.
65. Stanton BR, Leigh PN, Howard RJ, Barker GJ, Brown RG. Behavioural and emotional symptoms of apathy are associated with distinct patterns of brain atrophy in neurodegenerative disorders. J Neurol 2013; 260: 2481-90.
66. Starkstein SE, Ingram L, Garau ML, Mizrahi R. On the overlap between apathy and depression in dementia. J Neurol Neurosurg Psychiatry 2005; 76: 1070-4.
67. Tang WK, Chen YK, Lu JY, Chu WCW, Mok VCT, Ungvari GS, et al. White matter hyperintensities in post-stroke depression: a case control study. J Neurol Neurosurg Psychiatry 2010; 81: 1312-15.
68. Taylor WD, Aizenstein HJ, Alexopoulos GS. The vascular depression hypothesis: mechanisms linking vascular disease with depression [Internet]. Mol Psychiatry 2013; 18: 963-74.
69. Thobois S, Lhommée E, Klinger H, Ardouin C, Schmitt E, Bichon A, et al. Parkinsonian apathy responds to dopaminergic stimulation of D2/D3 receptors with piribedil. Brain 2013; 136: 1568-77.
70. Tuladhar AM, van Norden AGW, de Laat KF, Zwiers MP, van Dijk EJ, Norris DG, et al. White matter integrity in small vessel disease is related to cognition [Internet]. Neuroimage Clin 2015; 7: 518-24.
71. Uher R, Payne JL, Pavlova B, Perlis RH. Major depressive disorder in DSM-5: implications for clinical practice and research of changes from DSM-IV. Depress Anxiety 2013; 31: 459-71.
72. van der Mast RC, Vinkers DJ, Stek ML, Bek MC, Westendorp RGJ, Gussekloo J, et al. Vascular disease and apathy in old age. The Leiden 85-plus Study. Int J Geriatr Psychiatry 2008; 23: 266-71.
73. van Norden AGW, De Laat KF, Van Dijk EJ, van Uden IWM, Van Oudheusden LJB, Gons RAR, et al. Diffusion tensor imaging and cognition in cerebral small vessel disease. The RUN DMC study. Biochim Biophys Acta Mol Basis Dis 2012; 1822: 401-7.
74. van Uden IWM, Tuladhar AM, de Laat KF, van Norden AGW, Norris DG, van Dijk EJ, et al. White matter integrity and depressive symptoms in cerebral small vessel disease: The RUN DMC study. Am J Geriatr Psychiatry 2015; 23: 525-35.
75. Wen MC, Steffens DC, Chen MK, Zainal NH. Diffusion tensor imaging studies in late-life depression: systematic review and metaanalysis [Internet]. Int J Geriatr Psychiatry 2014; 29: 1173-84.
76. White CL, McClure LA, Wallace PM, Braimah J, Liskay A, Roldan A, et al. The correlates and course of depression in patients with lacunar stroke: results from the secondary prevention of small subcortical strokes (SPS3) study. Cerebrovasc Dis 2011; 32: 354-60.
77. Williams LS, Weinberger M, Harris LE, Clark DO, Biller J. Development of a stroke-specific quality of life scale. Stroke 1999; 30: 1362-9.
78. Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE. Permutation inference for the general linear model. Neuroimage 2014; 92: 381-97.
79. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, et al. Development and validation of a geriatric depression screening scale: a preliminary report [Internet]. J Psychiatr Res 1983; 17: 37-49.
80. Yuen GS, Gunning FM, Woods E, Klimstra SA, Hoptman MJ, Alexopoulos GS. Neuroanatomical correlates of apathy in late-life depression and antidepressant treatment response. J Affect Disord 2014; 166: 179-86.