Apathy is associated with white matter abnormalities in anterior, medial brain regions in persons with HIV infection

Journal of Clinical and Experimental Neuropsychology

Volumn 36, Issue 8, 2014, Pages 854-866

  Kamat, Rujvi ^a   Brown, Gregory G ^b,c   Bolden, Khalima ^a   Fennema Notestein, Christine ^b   Archibald, Sarah ^b   Marcotte, Thomas D ^b   Letendre, Scott L ^d   Ellis, Ronald J ^e   Woods, Steven Paul ^b   Grant, Igor ^b   Heaton, Robert K ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apathy; Depression; Diffusion tensor imaging; HIV AIDS; Prefrontal cortex

Indexed keywords

ADULT; APATHY; COHORT ANALYSIS; COMPLICATION; DIFFUSION TENSOR IMAGING; FEMALE; FRONTAL LOBE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LEUKOENCEPHALOPATHIES; MALE; MIDDLE AGED; NONPARAMETRIC TEST; PATHOLOGY; PSYCHOLOGICAL RATING SCALE; PSYCHOLOGY; REGRESSION ANALYSIS; VIROLOGY;

ADULT; APATHY; COHORT STUDIES; DIFFUSION TENSOR IMAGING; FEMALE; FRONTAL LOBE; HIV INFECTIONS; HUMANS; LEUKOENCEPHALOPATHIES; MALE; MIDDLE AGED; PSYCHIATRIC STATUS RATING SCALES; REGRESSION ANALYSIS; STATISTICS, NONPARAMETRIC;

EID: 84922516022     PISSN: 13803395     EISSN: 1744411X     Source Type: Journal    
DOI: 10.1080/13803395.2014.950636     Document Type: Article

References (65)

1. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.
2. Archibald, S. L., Masliah, E., Fennema-Notestine, C., Marcotte, T. D., Ellis, R. J., McCutchan, J. A., Jernigan, T. L. (2004). Correlation of in vivo neuroimaging abnormalities with postmortem human immunodeficiency virus encephalitis and dendritic loss. Archives of Neurology, 61(3), 369-376.
3. Aylward, E. H., Henderer, J. D., McArthur, J. C, Brettschneider, P. D., Harris, G. J., Barta, P. E., & Pearlson, G. D. (1993). Reduced basal ganglia volume in HIV-1-associated dementia: Results from quantitative neuroimaging. Neurology, 43(10), 2099-2104.
4. Barclay, T. R., Hinkin, C. H., & Castellon, S. A. (2007). Age-associated predictors of medication adherence in HIV-positive adults: Health beliefs, self-efficacy, and neurocognitive status. Health Psychology, 26(1), 40-49. doi:10.1037/0278-6133.26.1.40
5. Bonelli, R. M., & Cummings, J. L. (2007). Frontal-sub-cortical circuitry and behavior. Dialogues in Clinical Neuroscience, 9, 141-151.
6. Brown, C. A., Campbell, M. C, Karimi, M., Tabbal, S. D., Loftin, S. K., Tian, L. L., Perlmutter, J. S. (2012). Dopamine pathway loss in nucleus accumbens and ventral tegmental area predicts apathetic behavior in MPTP-lesioned monkeys. Experimental Neurology, 236(1), 190-197.
7. Castellon, S. A., Hinkin, C. H., & Myers, H. F. (2001). Neuropsychiatric alterations and neurocognitive performance in HIV/AIDS: A response to C. Bungener and R. Jouvent. [Letter]. Journal of the International Neuropsychological Society, 7(6), 776-777. doi: 10.1017/s1355617701766143
8. Castellon, S. A., Hinkin, C. H., Wood, S., & Yarema, K. T. (1998). Apathy, depression, and cognitive performance in HIV-1 infection. Journal of Neuropsychiatry and Clinical Neurosciences, 10(3), 320-329.
9. Catani, M., & de Schotten, M. T. (2012). Atlas of human brain connections. New York, NY: Oxford University Press.
10. Chen, Y., An, H, Zhu, H, Stone, T., Smith, J. K., Hall, C, Lin, W. (2009). White matter abnormalities revealed by diffusion tensor imaging in non-demented and demented HIV+ patients. NeuroImage, 47(4), 1154-1162.
11. Chiang, M. C, Dutton, R. A., Hayashi, K. M., Lopez, O. L., Aizenstein, H. J., Toga, A. W., Thompson, P. M. (2007). 3D pattern of brain atrophy in HIV/AIDS visualized using tensor-based morphometry. NeuroImage, 34(1), 44-60.
12. Choi, S. J., Lim, K. O., Monteiro, I., & Reisberg, B. (2005). Diffusion tensor imaging of frontal white matter microstructure in early Alzheimer's disease: A preliminary study. Journal of Geriatric Psychiatry and Neurology, 18(1), 12-19.
13. Cohen, R. A., Harezlak, J., Schifitto, G, Hana, G, Clark, U., Gongvatana, A., Navia, B. (2010). Effects of nadir CD4 count and duration of human immunodeficiency virus infection on brain volumes in the highly active antiretroviral therapy era. Journal of Neurovirology, 16(1), 25-32.
14. Cummings, J. L. (1993). Frontal-subcortical circuits and human behavior. Archives of Neurology, 50(8), 873.
15. Cummings, J. L., Mega, M., Gray, K., Rosenberg-Thompson, S., Carusi, D. A., & Gornbein, J. (1994). The Neuropsychiatric Inventory comprehensive assessment of psychopathology in dementia. Neurology, 44(12), 2308-2314.
16. De Cock, K. M., Crowley, S. P., Lo, Y.-R., Granich, R. M., & Williams, B. G. (2009). Preventing HIV transmission with antiretrovirals. Bulletin of the World Health Organization, 87(7), 488-488A.
17. Demirtas-Tatlidede, A., Bahar, S. Z., & Gurvit, H. (2013). Akinetic mutism without a structural prefrontal lesion. Cognitive and Behavioral Neurology, 26(2), 59-62.
18. Donner, A., & Zou, G. (2002). Testing the equality of dependent intraclass correlation coefficients. Journal of the Royal Statistical Society: Series D (The Statistician), 51(3), 367-379.
19. Everall, I., Vaida, F., Khanlou, N., Lazzaretto, D., Achim, C., Letendre, S., Masliah, E. (2009). Cliniconeuropathologic correlates of human immunodeficiency virus in the era of antiretroviral therapy. Journal of Neurovirology, 15(5-6), 360-370.
20. Filippi, C. G., Uluʇ, A. M., Ryan, E., Ferrando, S. J., & van Gorp, W. (2001). Diffusion tensor imaging of patients with HIV and normal-appearing white matter on MR images of the brain. American Journal of Neuroradiology, 22(2), 277-283.
21. Gongvatana, A., Schweinsburg, B. C., Taylor, M. J., Theilmann, R. J., Letendre, S. L., Alhassoon, O. M., CHARTER Group. (2009). White matter tract injury and cognitive impairment in human immunodeficiency virus-infected individuals. Journal of Neurovirology, 15(2), 187-195.
22. Grace, J., & Malloy, P. F. (2001). Frontal systems behavior scale (FrSBe): Professional manual. Lutz, FL: Psychological Assessment Resources.
23. Grunsfeld, A. A., & Login, I. S. (2006). Abulia following penetrating brain injury during endoscopic sinus surgery with disruption of the anterior cingulate circuit: Case report. BMC Neurology, 6(1), 4.
24. Hanssen, M., Peeters, F., Krabbendam, L., Radstake, S., Verdoux, H., & Van Os, J. (2003). How psychotic are individuals with non-psychotic disorders? Social Psychiatry and Psychiatric Epidemiology, 38(3), 149-154.
25. Hoare, J., Fouche, J. P., Spottiswoode, B., Joska, J., Schoeman, R., Stein, D., & Carey, P. (2010). White matter correlates of apathy in HIV-positive subjects: A diffusion tensor imaging study. The Journal of Neuropsychiatry and Clinical Neurosciences, 22(3), 313-320.
26. Jernigan, T. L., Archibald, S. L., Fennema-Notestine, C., Taylor, M. J., Theilmann, R. J., Julaton, M. D., Grant, I. (2011). Clinical factors related to brain structure in HIV: The CHARTER study. Journal of Neurovirology, 17(3), 248-257.
27. Kamat, R., Woods, S. P., Marcotte, T. D., Ellis, R. J., & Grant, I. (2012). Implications of apathy for everyday functioning outcomes in persons living with HIV infection. Archives of Clinical Neuropsychology, 27 (5), 520-531.
28. Kringelbach, M. L., & Rolls, E. T. (2004). The functional neuroanatomy of the human orbitofrontal cortex: Evidence from neuroimaging and neuropsychology. Progress in Neurobiology, 72(5), 341-372.
29. Langford, D., Hurford, R., Hashimoto, M., Digicaylioglu, M., & Masliah, E. (2005). Signalling crosstalk in FGF2-mediated protection of endothelial cells from HIV-gp120. BMC Neuroscience, 6(1), 8.
30. Lavretsky, H., Ballmaier, M., Pham, D., Toga, A., & Kumar, A. (2007). Neuroanatomical characteristics of geriatric apathy and depression: A magnetic resonance imaging study. The American Journal of Geriatric Psychiatry: Official Journal of the American Association for Geriatric Psychiatry, 15(5), 386.
31. Levy, M. L., Cummings, J. L., Fairbanks, L. A., Masterman, D., Miller, B. L., Craig, A. H., Litvan, I. (1998). Apathy is not depression. The Journal of Neuropsychiatry and Clinical Neurosciences, 10(3), 314-319.
32. Levy, R. (2012). Apathy: A pathology of goal-directed behaviour. A new concept of the clinic and pathophysiology of apathy. Revue Neurologique, 168(8), 585-597.
33. Levy, R., & Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cerebral Cortex, 16(7), 916-928.
34. Marin, R. S., Fogel, B. S., Hawkins, J., Duffy, J., & Krupp, B. (1995). Apathy - A treatable syndrome. Journal of Neuropsychiatry and Clinical Neurosciences, 7(1), 23-30.
35. McCandliss, B. D. (2011). Microstructural properties of white matter tracts are linked to the efficiency of specific attention networks. In M. Posner (Ed.), Cognitive neuroscience of attention (pp. 187-197). New York, NY: Guilford Press.
36. Navia, B. A., Cho, E. S., Petito, C. K., & Price, R. W. (1986). The AIDS dementia complex: II. Neuropathology. Annals of Neurology, 19(6), 525-535.
37. Oishi, K., Faria, A. V., van Zijl, P. C, & Mori, S. (2010). MRI atlas of human white matter. Oxford: Academic Press.
38. Ozdener, H. (2005). Molecular mechanisms of HIV-1 associated neurodegeneration. Journal of Biosciences, 30(3), 391-405.
39. Paul, R., Flanigan, T. P., Tashima, K., Cohen, R., Lawrence, J., Alt, E., Hinkin, C. (2005). Apathy correlates with cognitive function but not CD4 status in patients with human immunodeficiency virus. The Journal of Neuropsychiatry and Clinical Neurosciences, 17(1), 114-118.
40. Paul, R. H., Brickman, A. M., Navia, B., Hinkin, C, Malloy, P. F., Jefferson, A. L., Flanigan, T. P. (2005). Apathy is associated with volume of the nucleus accumbens in patients infected with HIV. The Journal of Neuropsychiatry and Clinical Neurosciences, 17(2), 167-171.
41. Pfefferbaum, A., Rosenbloom, M. J., Adalsteinsson, E., & Sullivan, E. V. (2007). Diffusion tensor imaging with quantitative fibre tracking in HIV infection and alcoholism comorbidity: Synergistic white matter damage. Brain, 130(1), 48-64.
42. Phillips, S., Sangalang, V., & Sterns, G. (1987). Basal forebrain infarction: A clinicopathologic correlation. Archives of Neurology, 44(11), 1134.
43. Pomara, N, Crandall, D. T., Choi, S. J., Johnson, G, & Lim, K. O. (2001). White matter abnormalities in HIV-1 infection: A diffusion tensor imaging study. Psychiatry Research: Neuroimaging, 106(1), 15-24.
44. Rabkin, J. G, Ferrando, S. J., van Gorp, W., Rieppi, R., McElhiney, M., & Sewell, M. (2000). Relationships among apathy, depression, and cognitive impairment in HIV/AIDS. Journal of Neuropsychiatry and Clinical Neurosciences, 12(4), 451.
45. Ragin, A. B., Wu, Y., Storey, P., Cohen, B. A., Edelman, R. R., & Epstein, L. G. (2005). Diffusion tensor imaging of subcortical brain injury in patients infected with human immunodeficiency virus. Journal of Neurovirology, 11(3), 292-298.
46. Reijnders, J. S., Scholtissen, B., Weber, W. E., Aalten, P., Verhey, F. R., & Leentjens, A. F. (2010). Neuroanatomical correlates of apathy in Parkinson's disease: A magnetic resonance imaging study using voxel-based morphometry. Movement Disorders, 25 (14), 2318-2325.
47. Saad, Z. S., Glen, D. R., Chen, G, Beauchamp, M. S., Desai, R., & Cox, R. W. (2009). A new method for improving functional-to-structural MRI alignment using local Pearson correlation. NeuroImage, 44(3), 839.
48. Schmierer, K., Wheeler-Kingshott, C. A., Boulby, P. A., Scaravilli, F., Altmann, D. R., Barker, G. J. Miller, D. H. (2007). Diffusion tensor imaging of post mortem multiple sclerosis brain. NeuroImage, 35(2), 467-477.
49. Song, S.-K., Sun, S.-W., Ramsbottom, M. J., Chang, C, Russell, J., & Cross, A. H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage, 17 (3), 1429-1436.
50. Sousa, A. E., Carneiro, J., Meier-Schellersheim, M., Grossman, Z., & Victorino, R. M. (2002). CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. The Journal of Immunology, 169(6), 3400-3406.
51. Starkstein, S. E., Jorge, R., Mizrahi, R., & Robinson, R. G. (2006). A prospective longitudinal study of apathy in Alzheimer's disease. Journal of Neurology, Neurosurgery & Psychiatry, 77(1), 8-11. doi:10.1136/jnnp.2005.069575
52. Starkstein, S. E., Mizrahi, R., Capizzano, A. A., Acion, L., Brockman, S., & Power, B. D. (2009). Neuroimaging correlates of apathy and depression in Alzheimer's disease. Journal of Neuropsychiatry and Clinical Neurosciences, 21(3), 259-265.
53. StataCorp, L. P. (2011). Stata multivariate statistics reference manual. College Station, TX: Author.
54. Stebbins, G. T., Smith, C. A., Bartt, R. E., Kessler, H. A., Adeyemi, O. M., Martin, E., Moseley, M. E. (2007). HIV-associated alterations in normal-appearing white matter: A voxel-wise diffusion tensor imaging study. Journal of Acquired Immune Deficiency Syndromes, 46(5), 564-573.
55. Stuss, D. T., Van Reekum, R., & Murphy, K. J. (2000). Differentiation of states and causes of apathy. In J. C. Borod (Ed.), The neuropsychology of emotion. Series in affective science (Vol. XVIII, pp. 340-363). New York, NY: Oxford University Press.
56. Tanaka, K, Matsumoto, K, Mansouri, F. A., & Buckley, M. J. (2013). Functional division among monkey prefrontal areas in goal-directed behavior. In D. T. Stuss & R. T. Knight (Eds.), Principles of frontal lobe function (2nd ed., pp. 249-258). New York, NY: Oxford University Press.
57. Tate, D., Paul, R. H, Flanigan, T. P., Tashima, K, Nash, J., Adair, C, Cohen, R. A. (2003). The impact of apathy and depression on quality of life in patients infected with HIV. Aids Patient Care and STDs, 17(3), 115-120. doi:10.1089/108729103763807936
58. Tekin, S., & Cummings, J. L. (2002). Frontal-subcortical neuronal circuits and clinical neuropsychiatry: An update. Journal of Psychosomatic Research, 53(2), 647-654.
59. Tengvar, C, Johansson, B., & Sorensen, J. (2004). Frontal lobe and cingulate cortical metabolic dysfunction in acquired akinetic mutism: A PET study of the interval form of carbon monoxide poisoning. Brain Injury, 18(6), 615-625.
60. Thurnher, M. M., Castillo, M., Stadler, A., Rieger, A., Schmid, B., & Sundgren, P. C. (2005). Diffusion-tensor MR imaging of the brain in human immunodeficiency virus-positive patients. American Journal of Neuroradiology, 26(9), 2275-2281.
61. Tsujimoto, M., Senda, J., Ishihara, T., Niimi, Y., Kawai, Y., Atsuta, N., Sobue, G. (2011). Behavioral changes in early ALS correlate with voxel-based morphometry and diffusion tensor imaging. Journal of the Neurological Sciences, 307(1), 34-40.
62. Wheeler-Kingshott, C. A., & Cercignani, M. (2009). About axial and radial diffusivities. Magnetic Resonance in Medicine, 61(5), 1255-1260.
63. Wittchen, H. U., Robins, L. N., Cottler, L. B., Sartorius, N., Burke, J., & Regier, D. (1991). Cross-cultural feasibility, reliability and sources of variance of the Composite International Diagnostic Interview (CIDI). The Multicentre WHO/ADAMHA Field Trials. The British Journal of Psychiatry, 159(5), 645-653.
64. World Health Organization, & UNICEF. (2008). Towards universal access: Scaling up priority HIV/AIDS interventions in the health sector: Progress report 2008. Geneva: WHO.
65. Wu, Y., Storey, P., Cohen, B., Epstein, L., Edelman, R., & Ragin, A. (2006). Diffusion alterations in corpus callosum of patients with HIV. American Journal of Neuroradiology, 27(3), 656-660.