Effects of HIV and early life stress on amygdala morphometry and neurocognitive function

Journal of the International Neuropsychological Society

Volumn 18, Issue 4, 2012, Pages 657-668

  Clark, Uraina S ^a,b,c   Cohen, Ronald A ^a,b   Sweet, Lawrence H ^a,d   Gongvatana, Assawin ^a,b   Devlin, Kathryn N ^b   Hana, George N ^b   Westbrook, Michelle L ^b   Mulligan, Richard C ^a,d   Jerskey, Beth A ^a,d   White, Tara L ^c   Navia, Bradford ^e   Tashima, Karen T ^a,b  

^a BROWN UNIVERSITY   (United States)

^b MIRIAM HOSPITAL   (United States)

^c BROWN UNIVERSITY   (United States)

^d BUTLER HOSPITAL   (United States)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amygdala; Cognition; HIV; Neuroimaging; Stress

Indexed keywords

EID: 84863690516     PISSN: 13556177     EISSN: 14697661     Source Type: Journal    
DOI: 10.1017/S1355617712000434     Document Type: Article

References (110)

1. Adimora, A.A., Schoenbach, V.J., Martinson, F.E., Coyne-Beasley, T., Doherty, I., Stancil, T.R., & Fullilove, R.E. (2006). Heterosexually transmitted HIV infection among African Americans in North Carolina. Journal of Acquired Immune Deficiency Syndromes, 41(5), 616-623.
2. Alemán-Gómez, Y., Melie-García, L., & Valdés-Hernández, P. (2006, June 11-15). IBASPM: Toolbox for automatic parcellation of brain structures. Paper presented at the 12th Annual Meeting of the Organization for Human Brain Mapping, Florence, Italy.
3. Amaral, D.G., & Price, J.L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). Journal of Comparative Neurology, 230(4), 465-496.
4. Ances, B.M., Roc, A.C., Wang, J., Korczykowski, M., Okawa, J., Stern, J., yDetre, J.A. (2006). Caudate blood flow and volume are reduced in HIV1 neurocognitively impaired patients. Neurology, 66(6), 862-866.
5. Andersen, S.L., Tomada, A., Vincow, E.S., Valente, E., Polcari, A., & Teicher, M.H. (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. Journal of Neuropsychiatry and Clinical Neurosciences, 20(3), 292-301.
6. 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, 2099-2104.
7. Baram, T.Z., & Hatalski, C.G. (1998). Neuropeptide-mediated excitability: A key triggering mechanism for seizure generation in the developing brain. Trends in Neurosciences, 21(11), 471-476.
8. Barbas, H., & De Olmos, J. (1990). Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey. Journal of Comparative Neurology, 300(4), 549-571.
9. Becker, J., Sanders, J., Madsen, S., Ragin, A., Kingsley, L., Maruca, V., y Thompson, P. (2011). Subcortical brain atrophy persists even in HAART-regulated HIV disease. Brain Imaging and Behavior, 5(2), 77-85.
10. Benedict, R.H.B., Schretlen, D., Groninger, L., & Brandt, J. (1998). Hopkins Verbal Learning Test-Revised: Normative data and analysis of inter-form and test-retest reliability. Clinical Neuropsychologist, 12(1), 43-55.
11. Blair, K.S., Smith, B.W., Mitchell, D.G., Morton, J., Vythilingam, M., Pessoa, L., yBlair, R.J. (2007). Modulation of emotion by cognition and cognition by emotion. Neuroimage, 35(1), 430-440.
12. Borkowski, J.G., Benton, A.L., & Spreen, O. (1967). Word fluency and brain damage. Neuropsychologia, 5(2), 135-140.
13. Boyce, W.T., Adams, S., Tschann, J.M., Cohen, F., Wara, D., & Gunnar, M.R. (1995). Adrenocortical and behavioral predictors of immune responses to starting school. Pediatric Research, 38(6), 1009-1017.
14. Brandt, J., & Benedict, R. (2001). Hopkins Verbal Learning Test-Revised. Professional Manual. Lutz, FL: Psychological Assessment Resources, Inc.
15. Brown, R. (2000). An introduction to neuroendocrinology. Cambridge, UK: Cambridge University Press.
16. Cardenas, V., Meyerhoff, D., Studholme, C., Kornak, J., Rothlind, J., Lampiris, H., y Weiner, M. (2009). Evidence for ongoing brain injury in human immunodeficiency virus-positive patients treated with antiretroviral therapy. Journal of Neurovirology, 15(4), 324-333.
17. Castelo, J.M., Courtney, M.G., Melrose, R.J., & Stern, C.E. (2007). Putamen hypertrophy in nondemented patients with human immunodeficiency virus infection and cognitive compromise. Archives of Neurology, 64(9), 1275-1280.
18. Castelo, J.M., Sherman, S.J., Courtney, M.G., Melrose, R.J., & Stern, C.E. (2006). Altered hippocampal-prefrontal activation in HIV patients during episodic memory encoding. Neurology, 66(11), 1688-1695.
19. CDC. (2005). HIV Transmission among black women-North Carolina, 2004. Morbidity and Mortality Weekly Report, 54(04), 89-94.
20. Chen, E., Matthews, K.A., & Boyce, W.T. (2002). Socioeconomic differences in children's health: How and why do these relationships change with age? Psychological Bulletin, 128(2), 295-329.
21. Childs, E.A., Lyles, R.H., Selnes, O.A., Chen, B., Miller, E.N., Cohen, B.A., y McArthur, J.C. (1999). Plasma viral load and CD4 lymphocytes predict HIV-associated dementia and sensory neuropathy. Neurology, 52(3), 607-613.
22. Clark, U.S., & Cohen, R.A. (2010). Brain dysfunction in the era of combination antiretroviral therapy: Implications for the treatment of the aging population of HIV-infected individuals. Current Opinion in Investigational Drugs, 11(8), 884-900.
23. Clifford, D.B., Evans, S.R., Yang, Y., & Gulick, R.M. (2005). The neuropsychological and neurological impact of hepatitis C virus co-infection in HIV-infected subjects. AIDS, 19(Suppl 3), S64-S71.
24. Cohen, R.A., Grieve, S., Hoth, K.F., Paul,R.H., Sweet, L.,Tate,D.,y Williams, L.M. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry, 59(10), 975-982.
25. Cohen, R.A., Harezlak, J., Gongvatana, A., Buchthal, S., Schifitto, G., Clark, U., y Navia, B. (2010). Cerebral metabolite abnormalities in human immunodeficiency virus are associated with cortical and subcortical volumes. Journal of Neurovirology, 16(6), 435-444.
26. Cohen, R.A., Harezlak, J., Schifitto, G., Hana, G., Clark, U., Gongvatana, A.,yNavia, 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.
27. Cohen, R.A., Paul, R.H., Stroud, L., Gunstad, J., Hitsman, B.L., McCaffery, J., y Gordon, E. (2006). Early life stress and adult emotional experience: An international perspective. International Journal of Psychiatry in Medicine, 36(1), 35-52.
28. Cohen, S., Kamarck, T., & Mermelstein, R. (1983). A global measure of perceived stress. Journal of Health and Social Behavior, 24(4), 385-396.
29. Devlin, K.N., Gongvatana, A., Clark, U.S., Chasman, J.D., Westbrook, M.L., Tashima, K.T., y Cohen, R.A. (2012). Neurocognitive Effects of HIV, Hepatitis C, and Substance Use History. Journal of the International Neuropsychological Society, 18(1), 68-78.
30. DHHS. (2001). Mental health: Culture, race, and ethnicity. A supplement to mental health: A report of the Surgeon General. Washington, DC: US Department of Health and Human Services.
31. Dolan, R.J., & Vuilleumier, P. (2003). Amygdala automaticity in emotional processing. Annals of the New York Academy of Sciences, 985, 348-355.
32. Dong, M., Anda, R.F., Felitti, V.J., Dube, S.R., Williamson, D.F., Thompson, T.J., y Giles, W.H. (2004). The interrelatedness of multiple forms of childhood abuse, neglect, and household dysfunction. Child Abuse & Neglect, 28(7), 771-784.
33. Drevets, W.C., & Raichle, M.E. (1998). Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: Implications for interactions between emotion and cognition. Cognition and Emotion, 12(3), 353-385.
34. Dube, S.R., Felitti, V.J., Dong, M., Giles, W.H., & Anda, R.F. (2003). The impact of adverse childhood experiences on health problems: Evidence from four birth cohorts dating back to 1900. Preventive Medicine, 37(3), 268-277.
35. Eaton, W.W., & Muntaner, C. (1999). Socioeconomic stratification and mental disorder. In A.V. Horwitz & T.K. Scheid (Eds.), A handbook for the study of mental health: Social contexts, theories, and systems. (pp. 259-283). NewYork: Cambridge University Press.
36. Fama, R., Rosenbloom, M.J., Nichols, B.N., Pfefferbaum, A., & Sullivan, E.V. (2009). Working and episodic memory in HIV infection, alcoholism, and their comorbidity: Baseline and 1-year follow-up examinations. Alcoholism, Clinical and Experimental Research, 33(10), 1815-1824.
37. Felitti, V.J., Anda, R.F., Nordenberg, D., Williamson, D.F., Spitz, A.M., Edwards, V., y Marks, J.S. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. American Journal of Preventive Medicine, 14(4), 245-258.
38. Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189-198.
39. Ghashghaei, H.T., & Barbas, H. (2002). Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience, 115(4), 1261-1279.
40. Gilbert, R., Widom, C.S., Browne, K., Fergusson, D., Webb, E., & Janson, S. (2009). Burden and consequences of child maltreatment in high-income countries. Lancet, 373(9657), 68-81.
41. Glaser, R., Rice, J., Speicher, C.E., Stout, J.C., & Kiecolt-Glaser, J.K. (1986). Stress depresses interferon production by leukocytes concomitant with a decrease in natural killer cell activity. Behavioral Neuroscience, 100(5), 675-678.
42. Hader, S.L., Smith, D.K., Moore, J.S., & Holmberg, S.D. (2001). HIV infection in women in the United States: Status at the Millennium. JAMA, 285(9), 1186-1192.
43. Hall, M., Whaley, R., Robertson, K., Hamby, S., Wilkins, J., & Hall, C. (1996). The correlation between neuropsychological and neuroanatomic changes over time in asymptomatic and symptomatic HIV-1-infected individuals. Neurology, 46(6), 1697-1702.
44. Hardt, J., & Rutter, M. (2004). Validity of adult retrospective reports of adverse childhood experiences: Review of the evidence. Journal of child psychology and psychiatry, and allied disciplines, 45(2), 260-273.
45. Harezlak, J., Buchthal, S., Taylor, M., Schifitto, G., Zhong, J., Daar, E.,yNavia, B. (2011). Persistence of HIV-associated cognitive impairment, inflammation, and neuronal injury in era of highly active antiretroviral treatment. AIDS, 25(5), 625-633.
46. Hariri, A.R., Bookheimer, S.Y., & Mazziotta, J.C. (2000). Modulating emotional responses: Effects of a neocortical network on the limbic system. Neuroreport, 11(1), 43-48.
47. Heaton, R.K., Clifford, D.B., Franklin, D.R., Jr., Woods, S.P., Ake, C., Vaida, F.,yGrant, I. (2010). HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology, 75(23), 2087-2096.
48. Heaton, R.K., Franklin, D.R., Ellis, R.J., McCutchan, J.A., Letendre, S.L., Leblanc, S., y Grant, I. (2011). HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. Journal of Neurovirology, 17(1), 3-16.
49. Heaton, R.K., Grant, I., Butters, N., White, D.A., Kirson, D., Atkinson, J.H., y The HNRC Group. (1995). The HNRC 500-Neuropsychology of HIV infection at different disease stages. Journal of the International Neuropsychological Society, 1(3), 231-251.
50. Hedges, D.W., & Woon, F.L. (2011). Early-life stress and cognitive outcome. Psychopharmacology (Berl), 214(1), 121-130.
51. Jernigan, T.L., Archibald, S.L., Fennema-Notestine, C., Taylor, M.J., Theilmann, R.J., Julaton, M.D.,yGrant, I. (2011). Clinical factors related to brain structure in HIV: The CHARTER study. Journal of Neurovirology, 17, 248-257.
52. Jernigan, T.L., Archibald, S., Hesselink, J.R., Atkinson, J.H., Velin, R.A., McCutchan, J.A.,yGrant, I. (1993). Magnetic resonance imaging morphometric analysis of cerebral volume loss in human immunodeficiency virus infection. The HNRC Group. Archives of Neurology, 50(3), 250-255.
53. Kellogg, S.H., McHugh, P.F., Bell, K., Schluger, J.H., Schluger, R.P., LaForge, K.S.,yKreek, M.J. (2003). The Kreek-McHugh-Schluger-Kellogg scale: A new, rapid method for quantifying substance abuse and its possible applications. Drug and Alcohol Dependence, 69(2), 137-150.
54. Kikusui, T., & Mori, Y. (2009). Behavioural and neurochemical consequences of early weaning in rodents. Journal of Neuroendocrinology, 21(4), 427-431.
55. Klove, H. (1963). Grooved pegboard. Lafayette, IN: Lafayette Instruments.
56. Krueger, L.E., Wood, R.W., Diehr, P.H., & Maxwell, C.L. (1990). Poverty and HIV seropositivity: The poor are more likely to be infected. AIDS, 4(8), 811-814.
57. Ledoux, J., Lane, R.D., & Nadel, L. (2000). Cognitive-emotional interactions: Listen to the brain. In R.D. Lane, L. Nadel, & G.L. Ahern (Eds.), Cognitive neuroscience of emotion (pp. 129-155). New York, NY: Oxford University Press.
58. Leserman, J. (2003). HIV disease progression: Depression, stress, and possible mechanisms. Biological Psychiatry, 54(3), 295-306.
59. Leserman, J. (2008). Role of depression, stress, and trauma in HIV disease progression. Psychosomatic Medicine, 70(5), 539-545.
60. Liberzon, I., Phan, K.L.,Decker, L.R.,& Taylor, S.F. (2003). Extended amygdala and emotional salience:APET activation study of positive and negative affect. Neuropsychopharmacology, 28(4), 726-733.
61. Maheu, F.S., Dozier, M., Guyer, A.E., Mandell, D., Peloso, E., Poeth, K., y Ernst, M. (2010). A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cognitive, Affective & Behavioral Neuroscience, 10(1), 34-49.
62. Martin-Thormeyer, E.M., & Paul, R.H. (2009). Drug abuse and hepatitis C infection as comorbid features of HIV associated neurocognitive disorder: Neurocognitive and neuroimaging features. Neuropsychology Review, 19(2), 215-231.
63. Maughan, B., & Rutter, M. (1997). Retrospective reporting of childhood adversity: Issues in assessing long-term recall. Journal of Personality Disorders, 11(1), 19-33.
64. Mehta, M.A., Golembo, N.I., Nosarti, C., Colvert, E., Mota, A., Williams, S.C., y Sonuga-Barke, E.J. (2009). Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: The English and Romanian Adoptees study pilot. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 50(8), 943-951.
65. Melrose, R.J., Tinaz, S., Castelo, J.M., Courtney, M.G., & Stern, C.E. (2008). Compromised fronto-striatal functioning in HIV: An fMRI investigation of semantic event sequencing. Behavioural Brain Research, 188(2), 337-347.
66. Miller, G.E., Cohen, S., & Ritchey, A.K. (2002). Chronic psychological stress and the regulation of pro-inflammatory cytokines: A glucocorticoid-resistance model. Health Psychology, 21(6), 531-541.
67. Moore, D.J., Masliah, E., Rippeth, J.D., Gonzalez, R., Carey, C.L., Cherner, M., y Grant, I. (2006). Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS, 20(6), 879-887.
68. Ono, M., Kikusui, T., Sasaki, N., Ichikawa, M., Mori, Y., & Murakami-Murofushi, K. (2008). Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male Balb/c mice. Neuroscience, 156(4), 1103-1110.
69. Paul, R.H., Cohen, R., Navia, B., & Tashima, K. (2002). Relationships between cognition and structural neuroimaging findings in adults with human immunodeficiency virus type-1. Neuroscience and Biobehavioral Reviews, 26(3), 353-359.
70. Paul, R.H., Ernst, T., Brickman, A.M., Yiannoutsos, C.T., Tate, D.F., Cohen, R.A., & Navia, B.A. (2008). Relative sensitivity of magnetic resonance spectroscopy and quantitative magnetic resonance imaging to cognitive function among nondemented individuals infected with HIV. Journal of the International Neuropsychological Society, 14(5), 725-733.
71. Paul, R.H., Henry, L., Grieve, S.M., Guilmette, T.J., Niaura, R., Bryant, R.,yGordon, E. (2008). The relationship between early life stress and microstructural integrity of the corpus callosum in a non-clinical population. Neuropsychiatric Disease and Treatment, 4(1), 193-201.
72. Payne, C., Machado, C.J., Bliwise, N.G., & Bachevalier, J. (2010). Maturation of the hippocampal formation and amygdala in Macaca mulatta: A volumetric magnetic resonance imaging study. Hippocampus, 20(8), 922-935.
73. Pessoa, L. (2008). On the relationship between emotion and cognition. Nature Reviews. Neuroscience, 9(2), 148-158.
74. Pessoa, L. (2010). Emergent processes in cognitive-emotional interactions. Dialogues in Clinical Neuroscience, 12(4), 433-448.
75. Petito, C.K., Roberts, B., Cantando, J.D., Rabinstein, A., & Duncan, R. (2001). Hippocampal injury and alterations in neuronal chemokine co-receptor expression in patients with AIDS. Journal of Neuropathology and Experimental Neurology, 60(4), 377-385.
76. Price, J.L. (2003). Comparative aspects of amygdala connectivity. Annals of the New York Academy of Sciences, 985, 50-58.
77. Quirk, G.J., Likhtik, E., Pelletier, J.G., & Pare, D. (2003). Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. Journal of Neuroscience, 23(25), 8800-8807.
78. Radloff, L.S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1(3), 385-401.
79. Reitan, R.M., & Davison, L.A. (1974). Clinical neuropsychology: Current status and applications. Oxford, England: V.H. Winston & Sons.
80. Repetti, R.L., Taylor, S.E., & Seeman, T.E. (2002). Risky families: Family social environments and the mental and physical health of offspring. Psychological Bulletin, 128(2), 330-366.
81. Rippeth, J.D., Heaton, R.K., Carey, C.L., Marcotte, T.D., Moore, D.J., Gonzalez, R., y Grant, I. (2004). Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. Journal of the International Neuropsychological Society, 10(1), 1-14.
82. Sa, M.J., Madeira, M.D., Ruela, C., Volk, B., Mota-Miranda, A., & Paula-Barbosa, M.M. (2004). Dendritic changes in the hippocampal formation of AIDS patients: A quantitative Golgi study. Acta Neuropathologica, 107(2), 97-110.
83. Salzberg, M., Kumar, G., Supit, L., Jones, N.C., Morris, M.J., Rees, S., & O'Brien, T.J. (2007). Early postnatal stress confers enduring vulnerability to limbic epileptogenesis. Epilepsia, 48(11), 2079-2085.
84. Schulte, T., Mueller-Oehring, E.M., Rosenbloom, M.J., Pfefferbaum, A., & Sullivan, E.V. (2005). Differential effect of HIV infection and alcoholism on conflict processing, attentional allocation, and perceptual load: Evidence from a Stroop Matchto-Sample task. Biological Psychiatry, 57(1), 67-75.
85. Seckfort, D.L., Paul, R., Grieve, S.M., Vandenberg, B., Bryant, R.A., Williams, L.M.,yGordon, E. (2008). Early life stress on brain structure and function across the lifespan: A preliminary study. Brain Imaging and Behavior, 2(1), 49-58.
86. Smith, G.D., Hart, C., Blane, D., & Hole, D. (1998). Adverse socioeconomic conditions in childhood and cause specific adult mortality: Prospective observational study. BMJ, 316(7145), 1631-1635.
87. Spreen, O., & Strauss, E. (1998). A compendium of neuropsychological tests: Administration, norms, and commentary (2nd ed.). New York, NY: Oxford University Press.
88. St Louis, M.E., Conway, G.A., Hayman, C.R., Miller, C., Petersen, L.R., & Dondero, T.J. (1991). Human immunodeficiency virus infection in disadvantaged adolescents. Findings from the US Job Corps. JAMA, 266(17), 2387-2391.
89. Stefanacci, L., Suzuki, W.A., & Amaral, D.G. (1996). Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. Journal of Comparative Neurology, 375(4), 552-582.
90. Stein, J.L., Wiedholz, L.M., Bassett, D.S., Weinberger, D.R., Zink, C.F., Mattay, V.S., & Meyer-Lindenberg, A. (2007). A validated network of effective amygdala connectivity. Neuroimage, 36(3), 736-745.
91. Stein, M.B., Koverola, C., Hanna, C., Torchia, M.G., & McClarty, B. (1997). Hippocampal volume in women victimized by childhood sexual abuse. Psychological Medicine, 27(4), 951-959.
92. Taylor, S.E. (2010). Mechanisms linking early life stress to adult health outcomes. Proceedings of the National Academy of Sciences of the United States of America, 107(19), 8507-8512.
93. Tomalski, P., & Johnson, M.H. (2010). The effects of early adversity on the adult and developing brain. Current Opinion in Psychiatry, 23(3), 233-238.
94. Tombaugh, T.N. (2004). Trail Making Test A and B: Normative data stratified by age and education. Archives of Clinical Neuropsychology, 19(2), 203-214.
95. Tottenham, N., Hare, T.A., Quinn, B.T., McCarry, T.W., Nurse, M., Gilhooly, T., y Casey, B.J. (2009). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13(1), 46-61.
96. Tottenham, N., & Sheridan, M.A. (2010). A review of adversity, the amygdala and the hippocampus: A consideration of developmental timing. Frontiers in Human Neuroscience, 3, 68.
97. Towgood, K.J., Pitkanen, M., Kulasegaram, R., Fradera, A., Kumar, A., Soni, S., y Kopelman, M.D. (2012). Mapping the brain in younger and older asymptomatic HIV-1 men: Frontal volume changes in the absence of other cortical or diffusion tensor abnormalities. Cortex, 48(2), 230-241.
98. Tran, T.T., Srivareerat, M., & Alkadhi, K.A. (2010). Chronic psychosocial stress triggers cognitive impairment in a novel atrisk model of Alzheimer's disease. Neurobiology of Disease, 37(3), 756-763.
99. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., y Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273-289.
100. Valcour, V.G., Yee, P., Williams, A.E., Shiramizu, B., Watters, M., Selnes, O.,ySacktor, N. (2006). Lowest ever CD4 lymphocyte count (CD4 nadir) as a predictor of current cognitive and neurological status in human immunodeficiency virus type 1 infection-The Hawaii Aging with HIV Cohort. Journal of Neurovirology, 12(5), 387-391.
101. Vyas, A., Pillai, A.G., & Chattarji, S. (2004). Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience, 128(4), 667-673.
102. Weathers, F., Litz, B., Herman, D., Huska, J., & Keane, T. (1993). The PTSD Checklist (PCL): Reliability, validity, and diagnostic utility. Paper presented at the Annual Convention of the International Society for Traumatic Stress Studies, San Antonio, TX.
103. Wechsler, D. (1997). WAIS-III administration and scoring manual. San Antonio, TX: Psychological Corporation.
104. Wechsler, D. (2001). Wechsler test of adult reading. San Antonio, TX: The Psychological Corporation.
105. Wenzel, S.L., & Tucker, J.S. (2005). Reemphasizing the context of women's risk for HIV/AIDS in the United States. Womens Health Issues, 15(4), 154-156.
106. Wiley, C.A., Achim, C.L., Christopherson, C., Kidane, Y., Kwok, S., Masliah, E.,ySoontornniyomkij, V. (1999). HIV mediates a productive infection of the brain. AIDS, 13(15), 2055-2059.
107. Wilson, R.S., Arnold, S.E., Schneider, J.A., Kelly, J.F., Tang, Y., & Bennett, D.A. (2006). Chronic psychological distress and risk of Alzheimer's disease in old age. Neuroepidemiology, 27(3), 143-153.
108. Yamasaki, H., LaBar, K.S., & McCarthy, G. (2002). Dissociable prefrontal brain systems for attention and emotion. Proceedings of the National Academy of Sciences of the United States of America, 99(17), 11447-11451.
109. Yun, R.J., Krystal, J.H., & Mathalon, D.H. (2010). Working memory overload: Fronto-limbic interactions and effects on subsequent working memory function. Brain Imaging and Behavior, 4(1), 96-108.
110. Zachariae, R. (2009). Psychoneuroimmunology: A bio-psychosocial approach to health and disease. Scandinavian Journal of Psychology, 50(6), 645-651.