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Effects of HIV and Early Life Stress on Amygdala Morphometry and Neurocognitive Function

Published online by Cambridge University Press:  24 May 2012

Uraina S. Clark*
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island Center for Alcohol and Addiction Studies, Department of Behavioral and Social Sciences, Brown University, Providence, Rhode Island
Ronald A. Cohen
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island
Lawrence H. Sweet
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Neuroimaging Center, Butler Hospital, Providence, Rhode Island
Assawin Gongvatana
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island
Kathryn N. Devlin
Affiliation:
Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island
George N. Hana
Affiliation:
Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island
Michelle L. Westbrook
Affiliation:
Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island Center for AIDS Research, The Miriam Hospital, Providence, Rhode Island
Richard C. Mulligan
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Neuroimaging Center, Butler Hospital, Providence, Rhode Island
Beth A. Jerskey
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Neuroimaging Center, Butler Hospital, Providence, Rhode Island
Tara L. White
Affiliation:
Center for Alcohol and Addiction Studies, Department of Behavioral and Social Sciences, Brown University, Providence, Rhode Island
Bradford Navia
Affiliation:
Tufts University School of Medicine, Boston, Massachusetts
Karen T. Tashima
Affiliation:
Center for AIDS Research, The Miriam Hospital, Providence, Rhode Island Department of Medicine, The Warren Alpert Medical School of Brown University, Providence, Rhode Island
*
Correspondence and reprint requests to: Uraina S. Clark, Center for Alcohol and Addiction Studies, Department of Behavioral and Social Sciences, Box G-S121-4, Brown University, Providence, RI 02912. E-mail: [email protected]

Abstract

Both HIV infection and high levels of early life stress (ELS) have been related to abnormalities in frontal-subcortical structures, yet the combined effects of HIV and ELS on brain structure and function have not been previously investigated. In this study we assessed 49 non-demented HIV-seropositive (HIV+) and 47 age-matched HIV-seronegative healthy control (HC) adults. Levels of ELS exposure were quantified and used to define four HIV-ELS groups: HC Low-ELS (N = 20); HC High-ELS (N = 27); HIV+ Low-ELS (N = 24); HIV+ High-ELS (N = 25). An automated segmentation tool measured volumes of brain structures known to show HIV-related or ELS-related effects; a brief neurocognitive battery was administered. A significant HIV-ELS interaction was observed for amygdala volumes, which was driven by enlargements in HIV+ High-ELS participants. The HIV+ High-ELS group also demonstrated significant reductions in psychomotor/processing speed compared with HC Low-ELS. Regression analyses in the HIV+ group revealed that amygdala enlargements were associated with higher ELS, lower nadir CD4 counts, and reduced psychomotor/processing speed. Our results suggest that HIV infection and high ELS interact to increase amygdala volume, which is associated with neurocognitive dysfunction in HIV+ patients. These findings highlight the lasting neuropathological influence of ELS and suggest that high ELS may be a significant risk factor for neurocognitive impairment in HIV-infected individuals. (JINS, 2012, 19, 1–12)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2012

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References

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), 616623.CrossRefGoogle ScholarPubMed
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.Google Scholar
Amaral, D.G., Price, J.L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). Journal of Comparative Neurology, 230(4), 465496.Google Scholar
Ances, B.M., Roc, A.C., Wang, J., Korczykowski, M., Okawa, J., Stern, J., Detre, J.A. (2006). Caudate blood flow and volume are reduced in HIV+ neurocognitively impaired patients. Neurology, 66(6), 862866.CrossRefGoogle ScholarPubMed
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), 292301.CrossRefGoogle ScholarPubMed
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, 20992104.Google Scholar
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), 471476.Google Scholar
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), 549571.Google Scholar
Becker, J., Sanders, J., Madsen, S., Ragin, A., Kingsley, L., Maruca, V., Thompson, P. (2011). Subcortical brain atrophy persists even in HAART-regulated HIV disease. Brain Imaging and Behavior, 5(2), 7785.CrossRefGoogle ScholarPubMed
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), 4355.Google Scholar
Blair, K.S., Smith, B.W., Mitchell, D.G., Morton, J., Vythilingam, M., Pessoa, L., Blair, R.J. (2007). Modulation of emotion by cognition and cognition by emotion. Neuroimage, 35(1), 430440.Google Scholar
Borkowski, J.G., Benton, A.L., Spreen, O. (1967). Word fluency and brain damage. Neuropsychologia, 5(2), 135140.CrossRefGoogle Scholar
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), 10091017.CrossRefGoogle ScholarPubMed
Brandt, J., Benedict, R. (2001). Hopkins Verbal Learning Test-Revised. Professional Manual. Lutz, FL: Psychological Assessment Resources, Inc.Google Scholar
Brown, R. (2000). An introduction to neuroendocrinology. Cambridge, UK: Cambridge University Press.Google Scholar
Cardenas, V., Meyerhoff, D., Studholme, C., Kornak, J., Rothlind, J., Lampiris, H., Weiner, M. (2009). Evidence for ongoing brain injury in human immunodeficiency virus-positive patients treated with antiretroviral therapy. Journal of Neurovirology, 15(4), 324333.Google Scholar
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), 12751280.Google Scholar
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), 16881695.CrossRefGoogle ScholarPubMed
CDC. (2005). HIV Transmission among black women – North Carolina, 2004. Morbidity and Mortality Weekly Report, 54(04), 8994.Google Scholar
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), 295329.CrossRefGoogle ScholarPubMed
Childs, E.A., Lyles, R.H., Selnes, O.A., Chen, B., Miller, E.N., Cohen, B.A., McArthur, J.C. (1999). Plasma viral load and CD4 lymphocytes predict HIV-associated dementia and sensory neuropathy. Neurology, 52(3), 607613.Google Scholar
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), 884900.Google Scholar
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), S64S71.Google Scholar
Cohen, R.A., Grieve, S., Hoth, K.F., Paul, R.H., Sweet, L., Tate, D., Williams, L.M. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry, 59(10), 975982.Google Scholar
Cohen, R.A., Harezlak, J., Gongvatana, A., Buchthal, S., Schifitto, G., Clark, U., Navia, B. (2010). Cerebral metabolite abnormalities in human immunodeficiency virus are associated with cortical and subcortical volumes. Journal of Neurovirology, 16(6), 435444.Google Scholar
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), 2532.CrossRefGoogle ScholarPubMed
Cohen, R.A., Paul, R.H., Stroud, L., Gunstad, J., Hitsman, B.L., McCaffery, J., Gordon, E. (2006). Early life stress and adult emotional experience: An international perspective. International Journal of Psychiatry in Medicine, 36(1), 3552.Google Scholar
Cohen, S., Kamarck, T., Mermelstein, R. (1983). A global measure of perceived stress. Journal of Health and Social Behavior, 24(4), 385396.Google Scholar
Devlin, K.N., Gongvatana, A., Clark, U.S., Chasman, J.D., Westbrook, M.L., Tashima, K.T., Cohen, R.A. (2012). Neurocognitive Effects of HIV, Hepatitis C, and Substance Use History. Journal of the International Neuropsychological Society, 18(1), 6878.CrossRefGoogle ScholarPubMed
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.Google Scholar
Dolan, R.J., Vuilleumier, P. (2003). Amygdala automaticity in emotional processing. Annals of the New York Academy of Sciences, 985, 348355.Google Scholar
Dong, M., Anda, R.F., Felitti, V.J., Dube, S.R., Williamson, D.F., Thompson, T.J., Giles, W.H. (2004). The interrelatedness of multiple forms of childhood abuse, neglect, and household dysfunction. Child Abuse & Neglect, 28(7), 771784.CrossRefGoogle ScholarPubMed
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), 353385.Google Scholar
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), 268277.CrossRefGoogle ScholarPubMed
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. 259283). NewYork: Cambridge University Press.Google Scholar
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), 18151824.Google Scholar
Felitti, V.J., Anda, R.F., Nordenberg, D., Williamson, D.F., Spitz, A.M., Edwards, V., 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), 245258.Google Scholar
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), 189198.Google Scholar
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), 12611279.CrossRefGoogle ScholarPubMed
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), 6881.Google Scholar
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), 675678.CrossRefGoogle ScholarPubMed
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), 11861192.Google Scholar
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), 16971702.Google Scholar
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), 260273.CrossRefGoogle ScholarPubMed
Harezlak, J., Buchthal, S., Taylor, M., Schifitto, G., Zhong, J., Daar, E., Navia, B. (2011). Persistence of HIV-associated cognitive impairment, inflammation, and neuronal injury in era of highly active antiretroviral treatment. AIDS, 25(5), 625633.Google Scholar
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), 4348.Google Scholar
Heaton, R.K., Clifford, D.B., Franklin, D.R. Jr., Woods, S.P., Ake, C., Vaida, F., Grant, I. (2010). HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology, 75(23), 20872096.Google Scholar
Heaton, R.K., Franklin, D.R., Ellis, R.J., McCutchan, J.A., Letendre, S.L., Leblanc, S., 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), 316.Google Scholar
Heaton, R.K., Grant, I., Butters, N., White, D.A., Kirson, D., Atkinson, J.H., … The HNRC Group. (1995). The HNRC 500-Neuropsychology of HIV infection at different disease stages. Journal of the International Neuropsychological Society, 1(3), 231251.CrossRefGoogle ScholarPubMed
Hedges, D.W., Woon, F.L. (2011). Early-life stress and cognitive outcome. Psychopharmacology (Berl), 214(1), 121130.CrossRefGoogle ScholarPubMed
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, 248257.CrossRefGoogle Scholar
Jernigan, T.L., Archibald, S., Hesselink, J.R., Atkinson, J.H., Velin, R.A., McCutchan, J.A., Grant, I. (1993). Magnetic resonance imaging morphometric analysis of cerebral volume loss in human immunodeficiency virus infection. The HNRC Group. Archives of Neurology,, 50(3), 250255.Google Scholar
Kellogg, S.H., McHugh, P.F., Bell, K., Schluger, J.H., Schluger, R.P., LaForge, K.S., Kreek, 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), 137150.Google Scholar
Kikusui, T., Mori, Y. (2009). Behavioural and neurochemical consequences of early weaning in rodents. Journal of Neuroendocrinology, 21(4), 427431.Google Scholar
Klove, H. (1963). Grooved pegboard. Lafayette, IN: Lafayette Instruments.Google Scholar
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), 811814.Google Scholar
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. 129155). New York, NY: Oxford University Press.Google Scholar
Leserman, J. (2003). HIV disease progression: Depression, stress, and possible mechanisms. Biological Psychiatry, 54(3), 295306.Google Scholar
Leserman, J. (2008). Role of depression, stress, and trauma in HIV disease progression. Psychosomatic Medicine, 70(5), 539545.Google Scholar
Liberzon, I., Phan, K.L., Decker, L.R., Taylor, S.F. (2003). Extended amygdala and emotional salience: A PET activation study of positive and negative affect. Neuropsychopharmacology, 28(4), 726733.Google Scholar
Maheu, F.S., Dozier, M., Guyer, A.E., Mandell, D., Peloso, E., Poeth, K., 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), 3449.CrossRefGoogle ScholarPubMed
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), 215231.CrossRefGoogle ScholarPubMed
Maughan, B., Rutter, M. (1997). Retrospective reporting of childhood adversity: Issues in assessing long-term recall. Journal of Personality Disorders, 11(1), 1933.Google Scholar
Mehta, M.A., Golembo, N.I., Nosarti, C., Colvert, E., Mota, A., Williams, S.C., 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), 943951.CrossRefGoogle ScholarPubMed
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), 337347.CrossRefGoogle ScholarPubMed
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), 531541.Google Scholar
Moore, D.J., Masliah, E., Rippeth, J.D., Gonzalez, R., Carey, C.L., Cherner, M., Grant, I. (2006). Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS, 20(6), 879887.Google Scholar
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), 11031110.Google Scholar
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), 353359.Google Scholar
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), 725733.Google Scholar
Paul, R.H., Henry, L., Grieve, S.M., Guilmette, T.J., Niaura, R., Bryant, R., Gordon, 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), 193201.CrossRefGoogle Scholar
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), 922935.Google Scholar
Pessoa, L. (2008). On the relationship between emotion and cognition. Nature Reviews. Neuroscience,, 9(2), 148158.Google Scholar
Pessoa, L. (2010). Emergent processes in cognitive-emotional interactions. Dialogues in Clinical Neuroscience, 12(4), 433448.Google Scholar
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), 377385.Google Scholar
Price, J.L. (2003). Comparative aspects of amygdala connectivity. Annals of the New York Academy of Sciences, 985, 5058.CrossRefGoogle ScholarPubMed
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), 88008807.Google Scholar
Radloff, L.S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1(3), 385401.Google Scholar
Reitan, R.M., Davison, L.A. (1974). Clinical neuropsychology: Current status and applications. Oxford, England: V.H. Winston & Sons.Google Scholar
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), 330366.Google Scholar
Rippeth, J.D., Heaton, R.K., Carey, C.L., Marcotte, T.D., Moore, D.J., Gonzalez, R., Grant, I. (2004). Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. Journal of the International Neuropsychological Society, 10(1), 114.Google Scholar
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), 97110.Google Scholar
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), 20792085.CrossRefGoogle ScholarPubMed
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 Match-to-Sample task. Biological Psychiatry, 57(1), 6775.Google Scholar
Seckfort, D.L., Paul, R., Grieve, S.M., Vandenberg, B., Bryant, R.A., Williams, L.M., Gordon, E. (2008). Early life stress on brain structure and function across the lifespan: A preliminary study. Brain Imaging and Behavior, 2(1), 4958.Google Scholar
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), 16311635.Google Scholar
Spreen, O., Strauss, E. (1998). A compendium of neuropsychological tests: Administration, norms, and commentary (2nd ed.). New York, NY: Oxford University Press.Google Scholar
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), 23872391.CrossRefGoogle ScholarPubMed
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), 552582.Google Scholar
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), 736745.CrossRefGoogle ScholarPubMed
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), 951959.CrossRefGoogle ScholarPubMed
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), 85078512.Google Scholar
Tomalski, P., Johnson, M.H. (2010). The effects of early adversity on the adult and developing brain. Current Opinion in Psychiatry, 23(3), 233238.CrossRefGoogle ScholarPubMed
Tombaugh, T.N. (2004). Trail Making Test A and B: Normative data stratified by age and education. Archives of Clinical Neuropsychology, 19(2), 203214.Google Scholar
Tottenham, N., Hare, T.A., Quinn, B.T., McCarry, T.W., Nurse, M., Gilhooly, T., Casey, B.J. (2009). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13(1), 4661.Google Scholar
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.Google ScholarPubMed
Towgood, K.J., Pitkanen, M., Kulasegaram, R., Fradera, A., Kumar, A., Soni, S., 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), 230241.Google Scholar
Tran, T.T., Srivareerat, M., Alkadhi, K.A. (2010). Chronic psychosocial stress triggers cognitive impairment in a novel at-risk model of Alzheimer's disease. Neurobiology of Disease, 37(3), 756763.Google Scholar
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., 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), 273289.Google Scholar
Valcour, V.G., Yee, P., Williams, A.E., Shiramizu, B., Watters, M., Selnes, O., Sacktor, 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), 387391.Google Scholar
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), 667673.Google Scholar
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.Google Scholar
Wechsler, D. (1997). WAIS-III administration and scoring manual. San Antonio, TX: Psychological Corporation.Google Scholar
Wechsler, D. (2001). Wechsler test of adult reading. San Antonio, TX: The Psychological Corporation.Google Scholar
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), 154156.Google Scholar
Wiley, C.A., Achim, C.L., Christopherson, C., Kidane, Y., Kwok, S., Masliah, E., Soontornniyomkij, V. (1999). HIV mediates a productive infection of the brain. AIDS, 13(15), 20552059.CrossRefGoogle ScholarPubMed
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), 143153.Google Scholar
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), 1144711451.Google Scholar
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), 96108.Google Scholar
Zachariae, R. (2009). Psychoneuroimmunology: A bio-psycho-social approach to health and disease. Scandinavian Journal of Psychology, 50(6), 645651.Google Scholar