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Published in: Journal of NeuroVirology 4/2015

01-08-2015

The association of perceived stress and verbal memory is greater in HIV-infected versus HIV-uninfected women

Authors: Leah H. Rubin, Judith A. Cook, Kathleen M. Weber, Mardge H. Cohen, Eileen Martin, Victor Valcour, Joel Milam, Kathryn Anastos, Mary A. Young, Christine Alden, Deborah R. Gustafson, Pauline M. Maki

Published in: Journal of NeuroVirology | Issue 4/2015

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Abstract

In contrast to findings from cohorts comprised primarily of HIV-infected men, verbal memory deficits are the largest cognitive deficit found in HIV-infected women from the Women’s Interagency HIV Study (WIHS), and this deficit is not explained by depressive symptoms or substance abuse. HIV-infected women may be at greater risk for verbal memory deficits due to a higher prevalence of cognitive risk factors such as high psychosocial stress and lower socioeconomic status. Here, we investigate the association between perceived stress using the Perceived Stress Scale (PSS-10) and verbal memory performance using the Hopkins Verbal Learning Test (HVLT) in 1009 HIV-infected and 496 at-risk HIV-uninfected WIHS participants. Participants completed a comprehensive neuropsychological test battery which yielded seven cognitive domain scores, including a primary outcome of verbal memory. HIV infection was not associated with a higher prevalence of high perceived stress (i.e., PSS-10 score in the top tertile) but was associated with worse performance on verbal learning (p < 0.01) and memory (p < 0.001), as well as attention (p = 0.02). Regardless of HIV status, high stress was associated with poorer performance in those cognitive domains (p’s < 0.05) as well as processing speed (p = 0.01) and executive function (p < 0.01). A significant HIV by stress interaction was found only for the verbal memory domain (p = 0.02); among HIV-infected women only, high stress was associated with lower performance (p’s < 0.001). That association was driven by the delayed verbal memory measure in particular. These findings suggest that high levels of perceived stress contribute to the deficits in verbal memory observed in WIHS women.
Literature
go back to reference Alderson AL, Novack TA (2002) Neurophysiological and clinical aspects of glucocorticoids and memory: a review. J Clin Exp Neuropsychol 24:335–355PubMedCrossRef Alderson AL, Novack TA (2002) Neurophysiological and clinical aspects of glucocorticoids and memory: a review. J Clin Exp Neuropsychol 24:335–355PubMedCrossRef
go back to reference Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE (2005) Influence of HAART on HIV-related CNS disease and neuroinflammation. J Neuropathol Exp Neurol 64:529–536PubMed Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE (2005) Influence of HAART on HIV-related CNS disease and neuroinflammation. J Neuropathol Exp Neurol 64:529–536PubMed
go back to reference Armstrong GL, Wasley A, Simard EP, McQuillan GM, Kuhnert WL, Alter MJ (2006) The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 144:705–714PubMedCrossRef Armstrong GL, Wasley A, Simard EP, McQuillan GM, Kuhnert WL, Alter MJ (2006) The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 144:705–714PubMedCrossRef
go back to reference Bacon MC, von Wyl V, Alden C, Sharp G, Robison E, Hessol N, Gange S, Barranday Y, Holman S, Weber K, Young MA (2005) The Women’s Interagency HIV Study: an observational cohort brings clinical sciences to the bench. Clin Diagn Lab Immunol 12:1013–1019PubMedCentralPubMed Bacon MC, von Wyl V, Alden C, Sharp G, Robison E, Hessol N, Gange S, Barranday Y, Holman S, Weber K, Young MA (2005) The Women’s Interagency HIV Study: an observational cohort brings clinical sciences to the bench. Clin Diagn Lab Immunol 12:1013–1019PubMedCentralPubMed
go back to reference Bangasser DA, Shors TJ (2004) Acute stress impairs trace eye blink conditioning in females without altering the unconditioned response. Neurobiol Learn Mem 82:57–60PubMedCentralPubMedCrossRef Bangasser DA, Shors TJ (2004) Acute stress impairs trace eye blink conditioning in females without altering the unconditioned response. Neurobiol Learn Mem 82:57–60PubMedCentralPubMedCrossRef
go back to reference Barkan SE, Melnick SL, Preston-Martin S, Weber K, Kalish LA, Miotti P, Young M, Greenblatt R, Sacks H, Feldman J (1998) The Women’s Interagency HIV Study. WIHS Collaborative Study Group. Epidemiology 9:117–125PubMedCrossRef Barkan SE, Melnick SL, Preston-Martin S, Weber K, Kalish LA, Miotti P, Young M, Greenblatt R, Sacks H, Feldman J (1998) The Women’s Interagency HIV Study. WIHS Collaborative Study Group. Epidemiology 9:117–125PubMedCrossRef
go back to reference Benton AL (1968) Differential behavioral effects in frontal lobe disease. Neuropsychologia 6 Benton AL (1968) Differential behavioral effects in frontal lobe disease. Neuropsychologia 6
go back to reference Brandt J, Benedict RHB (2001) Hopkins verbal learning test revised. PAR, Odessa Brandt J, Benedict RHB (2001) Hopkins verbal learning test revised. PAR, Odessa
go back to reference Bremner JD, Vythilingam M, Vermetten E, Afzal N, Nazeer A, Newcomer JW, Charney DS (2004) Effects of dexamethasone on declarative memory function in posttraumatic stress disorder. Psychiatry Res 129:1–10PubMedCrossRef Bremner JD, Vythilingam M, Vermetten E, Afzal N, Nazeer A, Newcomer JW, Charney DS (2004) Effects of dexamethasone on declarative memory function in posttraumatic stress disorder. Psychiatry Res 129:1–10PubMedCrossRef
go back to reference Brief DJ, Bollinger AR, Vielhauer MJ, Berger-Greenstein JA, Morgan EE, Brady SM, Buondonno LM, Keane TM (2004) Understanding the interface of HIV, trauma, post-traumatic stress disorder, and substance use and its implications for health outcomes. AIDS Care 16(Suppl 1):S97–S120PubMedCrossRef Brief DJ, Bollinger AR, Vielhauer MJ, Berger-Greenstein JA, Morgan EE, Brady SM, Buondonno LM, Keane TM (2004) Understanding the interface of HIV, trauma, post-traumatic stress disorder, and substance use and its implications for health outcomes. AIDS Care 16(Suppl 1):S97–S120PubMedCrossRef
go back to reference Brooke SM, Sapolsky RM (2002) Glucocorticoid exacerbation of gp120 neurotoxicity: role of microglia. Exp Neurol 177:151–158PubMedCrossRef Brooke SM, Sapolsky RM (2002) Glucocorticoid exacerbation of gp120 neurotoxicity: role of microglia. Exp Neurol 177:151–158PubMedCrossRef
go back to reference Buwalda B, Kole MH, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas JM (2005) Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 29:83–97PubMedCrossRef Buwalda B, Kole MH, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas JM (2005) Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 29:83–97PubMedCrossRef
go back to reference Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–749PubMedCrossRef Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–749PubMedCrossRef
go back to reference Cohen M, Deamant C, Barkan S, Richardson J, Young M, Holman S, Anastos K, Cohen J, Melnick S (2000) Domestic violence and childhood sexual abuse in HIV-infected women and women at risk for HIV. Am J Public Health 90:560–565PubMedCentralPubMedCrossRef Cohen M, Deamant C, Barkan S, Richardson J, Young M, Holman S, Anastos K, Cohen J, Melnick S (2000) Domestic violence and childhood sexual abuse in HIV-infected women and women at risk for HIV. Am J Public Health 90:560–565PubMedCentralPubMedCrossRef
go back to reference Cohen RA, Grieve S, Hoth KF, Paul RH, Sweet L, Tate D, Gunstad J, Stroud L, McCaffery J, Hitsman B, Niaura R, Clark CR, McFarlane A, Bryant R, Gordon E, Williams LM (2006) Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol Psychiatry 59:975–982PubMedCrossRef Cohen RA, Grieve S, Hoth KF, Paul RH, Sweet L, Tate D, Gunstad J, Stroud L, McCaffery J, Hitsman B, Niaura R, Clark CR, McFarlane A, Bryant R, Gordon E, Williams LM (2006) Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol Psychiatry 59:975–982PubMedCrossRef
go back to reference Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24:385–396PubMedCrossRef Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24:385–396PubMedCrossRef
go back to reference Cohen S, Williamson G (1988) Perceived stress in a probability sample of the United States. In: Spacapan S, Oskamp S (eds) The social psychology of health: Claremont Symposium on applied social psychology. Sage, Newbury Park, CA Cohen S, Williamson G (1988) Perceived stress in a probability sample of the United States. In: Spacapan S, Oskamp S (eds) The social psychology of health: Claremont Symposium on applied social psychology. Sage, Newbury Park, CA
go back to reference Comalli PE, Wapner S, Werner H (1962) Interference effects of Stroop color-word test in childhood, adulthood, and aging. J Genet Psychol 100:47–53PubMedCrossRef Comalli PE, Wapner S, Werner H (1962) Interference effects of Stroop color-word test in childhood, adulthood, and aging. J Genet Psychol 100:47–53PubMedCrossRef
go back to reference DeVries AC, Craft TK, Glasper ER, Neigh GN, Alexander JK (2007) 2006 Curt P. Richter award winner: social influences on stress responses and health. Psychoneuroendocrinology 32:587–603PubMedCrossRef DeVries AC, Craft TK, Glasper ER, Neigh GN, Alexander JK (2007) 2006 Curt P. Richter award winner: social influences on stress responses and health. Psychoneuroendocrinology 32:587–603PubMedCrossRef
go back to reference Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13:3839–3847PubMed Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13:3839–3847PubMed
go back to reference Gorman AA, Foley JM, Ettenhofer ML, Hinkin CH, van Gorp WG (2009) Functional consequences of HIV-associated neuropsychological impairment. Neuropsychol Rev 19:186–203PubMedCentralPubMedCrossRef Gorman AA, Foley JM, Ettenhofer ML, Hinkin CH, van Gorp WG (2009) Functional consequences of HIV-associated neuropsychological impairment. Neuropsychol Rev 19:186–203PubMedCentralPubMedCrossRef
go back to reference Grossman R, Yehuda R, Golier J, McEwen B, Harvey P, Maria NS (2006) Cognitive effects of intravenous hydrocortisone in subjects with PTSD and healthy control subjects. Ann N Y Acad Sci 1071:410–421PubMedCrossRef Grossman R, Yehuda R, Golier J, McEwen B, Harvey P, Maria NS (2006) Cognitive effects of intravenous hydrocortisone in subjects with PTSD and healthy control subjects. Ann N Y Acad Sci 1071:410–421PubMedCrossRef
go back to reference Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, Corkran SH, Duarte NA, Clifford DB, Woods SP, Collier AC, Marra CM, Morgello S, Mindt MR, Taylor MJ, Marcotte TD, Atkinson JH, Wolfson T, Gelman BB, McArthur JC, Simpson DM, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 17:3–16PubMedCentralPubMedCrossRef Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, Corkran SH, Duarte NA, Clifford DB, Woods SP, Collier AC, Marra CM, Morgello S, Mindt MR, Taylor MJ, Marcotte TD, Atkinson JH, Wolfson T, Gelman BB, McArthur JC, Simpson DM, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 17:3–16PubMedCentralPubMedCrossRef
go back to reference Heaton RK, Grant I, Matthews CG (1991) Comprehensive norms for an expanded Halstead-Reitan battery: demographic corrections, research findings, and clinical applications. Psychological Assessment Resources, Odessa, FL Heaton RK, Grant I, Matthews CG (1991) Comprehensive norms for an expanded Halstead-Reitan battery: demographic corrections, research findings, and clinical applications. Psychological Assessment Resources, Odessa, FL
go back to reference Hinkin CH, Castellon SA, Durvasula RS, Hardy DJ, Lam MN, Mason KI, Thrasher D, Goetz MB, Stefaniak M (2002) Medication adherence among HIV+ adults: effects of cognitive dysfunction and regimen complexity. Neurology 59:1944–1950PubMedCentralPubMedCrossRef Hinkin CH, Castellon SA, Durvasula RS, Hardy DJ, Lam MN, Mason KI, Thrasher D, Goetz MB, Stefaniak M (2002) Medication adherence among HIV+ adults: effects of cognitive dysfunction and regimen complexity. Neurology 59:1944–1950PubMedCentralPubMedCrossRef
go back to reference Hinkin CH, Hardy DJ, Mason KI, Castellon SA, Durvasula RS, Lam MN, Stefaniak M (2004) Medication adherence in HIV-infected adults: effect of patient age, cognitive status, and substance abuse. AIDS 18(Suppl 1):S19–S25PubMedCentralPubMedCrossRef Hinkin CH, Hardy DJ, Mason KI, Castellon SA, Durvasula RS, Lam MN, Stefaniak M (2004) Medication adherence in HIV-infected adults: effect of patient age, cognitive status, and substance abuse. AIDS 18(Suppl 1):S19–S25PubMedCentralPubMedCrossRef
go back to reference Hochhauser CJ, Gaur S, Marone R, Lewis M (2008) The impact of environmental risk factors on HIV-associated cognitive decline in children. AIDS Care 20:692–699PubMedCrossRef Hochhauser CJ, Gaur S, Marone R, Lewis M (2008) The impact of environmental risk factors on HIV-associated cognitive decline in children. AIDS Care 20:692–699PubMedCrossRef
go back to reference Johansson L, Guo X, Waern M, Ostling S, Gustafson D, Bengtsson C, Skoog I (2010) Midlife psychological stress and risk of dementia: a 35-year longitudinal population study. Brain 133:2217–2224PubMedCrossRef Johansson L, Guo X, Waern M, Ostling S, Gustafson D, Bengtsson C, Skoog I (2010) Midlife psychological stress and risk of dementia: a 35-year longitudinal population study. Brain 133:2217–2224PubMedCrossRef
go back to reference Johansson L, Skoog I, Gustafson DR, Olesen PJ, Waern M, Bengtsson C, Bjorkelund C, Pantoni L, Simoni M, Lissner L, Guo X (2012) Midlife psychological distress associated with late-life brain atrophy and white matter lesions: a 32-year population study of women. Psychosom Med 74:120–125PubMedCrossRef Johansson L, Skoog I, Gustafson DR, Olesen PJ, Waern M, Bengtsson C, Bjorkelund C, Pantoni L, Simoni M, Lissner L, Guo X (2012) Midlife psychological distress associated with late-life brain atrophy and white matter lesions: a 32-year population study of women. Psychosom Med 74:120–125PubMedCrossRef
go back to reference Kajantie E, Phillips DI (2006) The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31:151–178PubMedCrossRef Kajantie E, Phillips DI (2006) The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31:151–178PubMedCrossRef
go back to reference Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453–462PubMed Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453–462PubMed
go back to reference Kirschbaum C, Wolf OT, May M, Wippich W, Hellhammer DH (1996) Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci 58:1475–1483PubMedCrossRef Kirschbaum C, Wolf OT, May M, Wippich W, Hellhammer DH (1996) Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci 58:1475–1483PubMedCrossRef
go back to reference Kirschbaum C, Wust S, Hellhammer D (1992) Consistent sex differences in cortisol responses to psychological stress. Psychosom Med 54:648–657PubMedCrossRef Kirschbaum C, Wust S, Hellhammer D (1992) Consistent sex differences in cortisol responses to psychological stress. Psychosom Med 54:648–657PubMedCrossRef
go back to reference Kudielka BM, Kirschbaum C (2005) Sex differences in HPA axis responses to stress: a review. Biol Psychol 69:113–132PubMedCrossRef Kudielka BM, Kirschbaum C (2005) Sex differences in HPA axis responses to stress: a review. Biol Psychol 69:113–132PubMedCrossRef
go back to reference Li H, Li W, Wei D, Chen Q, Jackson T, Zhang Q, Qiu J (2014) Examining brain structures associated with perceived stress in a large sample of young adults via voxel-based morphometry. Neuroimage 92C:1–7CrossRef Li H, Li W, Wei D, Chen Q, Jackson T, Zhang Q, Qiu J (2014) Examining brain structures associated with perceived stress in a large sample of young adults via voxel-based morphometry. Neuroimage 92C:1–7CrossRef
go back to reference Luine V, Martinez C, Villegas M, Magarinos AM, McEwen BS (1996) Restraint stress reversibly enhances spatial memory performance. Physiol Behav 59:27–32PubMedCrossRef Luine V, Martinez C, Villegas M, Magarinos AM, McEwen BS (1996) Restraint stress reversibly enhances spatial memory performance. Physiol Behav 59:27–32PubMedCrossRef
go back to reference Lupien SJ, Fiocco A, Wan N, Maheu F, Lord C, Schramek T, Tu MT (2005) Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30:225–242PubMedCrossRef Lupien SJ, Fiocco A, Wan N, Maheu F, Lord C, Schramek T, Tu MT (2005) Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30:225–242PubMedCrossRef
go back to reference Lupien SJ, Lepage M (2001) Stress, memory, and the hippocampus: can’t live with it, can’t live without it. Behav Brain Res 127:137–158PubMedCrossRef Lupien SJ, Lepage M (2001) Stress, memory, and the hippocampus: can’t live with it, can’t live without it. Behav Brain Res 127:137–158PubMedCrossRef
go back to reference Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445PubMedCrossRef Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445PubMedCrossRef
go back to reference Magarinos AM, Somoza G, De Nicola AF (1987) Glucocorticoid negative feedback and glucocorticoid receptors after hippocampectomy in rats. Horm Metab Res 19:105–109PubMedCrossRef Magarinos AM, Somoza G, De Nicola AF (1987) Glucocorticoid negative feedback and glucocorticoid receptors after hippocampectomy in rats. Horm Metab Res 19:105–109PubMedCrossRef
go back to reference Maki PM, Cohen MH, Weber K, Little DM, Fornelli D, Rubin LH, Perschler P, Gould F, Martin E (2009) Impairments in memory and hippocampal function in HIV-positive vs HIV-negative women: a preliminary study. Neurology 72:1661–1668PubMedCentralPubMedCrossRef Maki PM, Cohen MH, Weber K, Little DM, Fornelli D, Rubin LH, Perschler P, Gould F, Martin E (2009) Impairments in memory and hippocampal function in HIV-positive vs HIV-negative women: a preliminary study. Neurology 72:1661–1668PubMedCentralPubMedCrossRef
go back to reference Maki PM, Rubin LH, Valcour V, Martin E, Crystal HA, Young M, Weber KM, Manly J, Richardson J, Alden C, Anastos K (2015) Cognitive function in women with HIV: findings from the Women’s Interagency HIV Study. Neurology 84(3):231–240 Maki PM, Rubin LH, Valcour V, Martin E, Crystal HA, Young M, Weber KM, Manly J, Richardson J, Alden C, Anastos K (2015) Cognitive function in women with HIV: findings from the Women’s Interagency HIV Study. Neurology 84(3):231–240
go back to reference Manly JJ, Jacobs DM, Touradji P, Small SA, Stern Y (2002) Reading level attenuates differences in neuropsychological test performance between African American and White elders. J Int Neuropsychol Soc 8:341–348PubMedCrossRef Manly JJ, Jacobs DM, Touradji P, Small SA, Stern Y (2002) Reading level attenuates differences in neuropsychological test performance between African American and White elders. J Int Neuropsychol Soc 8:341–348PubMedCrossRef
go back to reference Manly JJ, Smith C, Crystal HA, Richardson J, Golub ET, Greenblatt R, Robison E, Martin EM, Young M (2011) Relationship of ethnicity, age, education, and reading level to speed and executive function among HIV+ and HIV− women: the Women’s Interagency HIV Study (WIHS) Neurocognitive Substudy. J Clin Exp Neuropsychol 33:853–863PubMedCentralPubMedCrossRef Manly JJ, Smith C, Crystal HA, Richardson J, Golub ET, Greenblatt R, Robison E, Martin EM, Young M (2011) Relationship of ethnicity, age, education, and reading level to speed and executive function among HIV+ and HIV− women: the Women’s Interagency HIV Study (WIHS) Neurocognitive Substudy. J Clin Exp Neuropsychol 33:853–863PubMedCentralPubMedCrossRef
go back to reference Massad LS, Agniel D, Minkoff H, Watts DH, D’Souza G, Levine AM, Darragh TM, Young M, Cajigas A, Weber K (2011) Effect of stress and depression on the frequency of squamous intraepithelial lesions. J Low Genit Tract Dis 15:42–47PubMedCentralPubMedCrossRef Massad LS, Agniel D, Minkoff H, Watts DH, D’Souza G, Levine AM, Darragh TM, Young M, Cajigas A, Weber K (2011) Effect of stress and depression on the frequency of squamous intraepithelial lesions. J Low Genit Tract Dis 15:42–47PubMedCentralPubMedCrossRef
go back to reference McCormick CM, Lewis E, Somley B, Kahan TA (2007) Individual differences in cortisol levels and performance on a test of executive function in men and women. Physiol Behav 91:87–94PubMedCrossRef McCormick CM, Lewis E, Somley B, Kahan TA (2007) Individual differences in cortisol levels and performance on a test of executive function in men and women. Physiol Behav 91:87–94PubMedCrossRef
go back to reference McEwen BS (2000) Effects of adverse experiences for brain structure and function. Biol Psychiatry 48:721–731PubMedCrossRef McEwen BS (2000) Effects of adverse experiences for brain structure and function. Biol Psychiatry 48:721–731PubMedCrossRef
go back to reference McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904PubMedCrossRef McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904PubMedCrossRef
go back to reference McEwen BS, De Kloet ER, Rostene W (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66:1121–1188PubMed McEwen BS, De Kloet ER, Rostene W (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66:1121–1188PubMed
go back to reference Meaney MJ, Aitken DH (1985) [3H]Dexamethasone binding in rat frontal cortex. Brain Res 328:176–180PubMedCrossRef Meaney MJ, Aitken DH (1985) [3H]Dexamethasone binding in rat frontal cortex. Brain Res 328:176–180PubMedCrossRef
go back to reference Moore DJ, Masliah E, Rippeth JD, Gonzalez R, Carey CL, Cherner M, Ellis RJ, Achim CL, Marcotte TD, Heaton RK, Grant I (2006) Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS 20:879–887PubMedCrossRef Moore DJ, Masliah E, Rippeth JD, Gonzalez R, Carey CL, Cherner M, Ellis RJ, Achim CL, Marcotte TD, Heaton RK, Grant I (2006) Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS 20:879–887PubMedCrossRef
go back to reference Olver JS, Pinney M, Maruff P, Norman TR (2014) Impairments of spatial working memory and attention following acute psychosocial stress. Stress Health Olver JS, Pinney M, Maruff P, Norman TR (2014) Impairments of spatial working memory and attention following acute psychosocial stress. Stress Health
go back to reference Plessow F, Fischer R, Kirschbaum C, Goschke T (2011) Inflexibly focused under stress: acute psychosocial stress increases shielding of action goals at the expense of reduced cognitive flexibility with increasing time lag to the stressor. J Cogn Neurosci 23:3218–3227PubMedCrossRef Plessow F, Fischer R, Kirschbaum C, Goschke T (2011) Inflexibly focused under stress: acute psychosocial stress increases shielding of action goals at the expense of reduced cognitive flexibility with increasing time lag to the stressor. J Cogn Neurosci 23:3218–3227PubMedCrossRef
go back to reference Pukay-Martin ND, Cristiani SA, Saveanu R, Bornstein RA (2003) The relationship between stressful life events and cognitive function in HIV-infected men. J Neuropsychiatry Clin Neurosci 15:436–441PubMedCrossRef Pukay-Martin ND, Cristiani SA, Saveanu R, Bornstein RA (2003) The relationship between stressful life events and cognitive function in HIV-infected men. J Neuropsychiatry Clin Neurosci 15:436–441PubMedCrossRef
go back to reference Pukay-Martin ND, Pontoski KE, Maxwell MA, Calhoun PS, Dutton CE, Clancy CP, Hertzberg MA, Collie CF, Beckham JC (2012) The influence of depressive symptoms on suicidal ideation among U.S. Vietnam-era and Afghanistan/Iraq-era veterans with posttraumatic stress disorder. J Trauma Stress 25:578–582PubMedCentralPubMedCrossRef Pukay-Martin ND, Pontoski KE, Maxwell MA, Calhoun PS, Dutton CE, Clancy CP, Hertzberg MA, Collie CF, Beckham JC (2012) The influence of depressive symptoms on suicidal ideation among U.S. Vietnam-era and Afghanistan/Iraq-era veterans with posttraumatic stress disorder. J Trauma Stress 25:578–582PubMedCentralPubMedCrossRef
go back to reference Reitan R (1978) Manual for administration of neuropsychological test batteries for adults and children. Neuropsychology Laboratories, Inc., Tuscon, AZ Reitan R (1978) Manual for administration of neuropsychological test batteries for adults and children. Neuropsychology Laboratories, Inc., Tuscon, AZ
go back to reference Reitan R, Wolfson D (eds) (1985) The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. Neuropsychology Press, Tuscon, AZ Reitan R, Wolfson D (eds) (1985) The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. Neuropsychology Press, Tuscon, AZ
go back to reference Rubin LH, Sundermann EE, Cook JA, Martin EM, Golub ET, Weber KM, Cohen MH, Crystal H, Cederbaum JA, Anastos K, Young M, Greenblatt RM, Maki PM (2014) Investigation of menopausal stage and symptoms on cognition in human immunodeficiency virus-infected women. Menopause Rubin LH, Sundermann EE, Cook JA, Martin EM, Golub ET, Weber KM, Cohen MH, Crystal H, Cederbaum JA, Anastos K, Young M, Greenblatt RM, Maki PM (2014) Investigation of menopausal stage and symptoms on cognition in human immunodeficiency virus-infected women. Menopause
go back to reference Sanchez MM, Young LJ, Plotsky PM, Insel TR (2000) Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. J Neurosci 20:4657–4668PubMed Sanchez MM, Young LJ, Plotsky PM, Insel TR (2000) Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. J Neurosci 20:4657–4668PubMed
go back to reference Schoofs D, Pabst S, Brand M, Wolf OT (2013) Working memory is differentially affected by stress in men and women. Behav Brain Res 241:144–153PubMedCrossRef Schoofs D, Pabst S, Brand M, Wolf OT (2013) Working memory is differentially affected by stress in men and women. Behav Brain Res 241:144–153PubMedCrossRef
go back to reference Schoofs D, Preuss D, Wolf OT (2008) Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology 33:643–653PubMedCrossRef Schoofs D, Preuss D, Wolf OT (2008) Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology 33:643–653PubMedCrossRef
go back to reference Seeman TE, McEwen BS, Singer BH, Albert MS, Rowe JW (1997) Increase in urinary cortisol excretion and memory declines: MacArthur studies of successful aging. J Clin Endocrinol Metab 82:2458–2465PubMed Seeman TE, McEwen BS, Singer BH, Albert MS, Rowe JW (1997) Increase in urinary cortisol excretion and memory declines: MacArthur studies of successful aging. J Clin Endocrinol Metab 82:2458–2465PubMed
go back to reference Servatius RJ, Shors TJ (1994) Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav Neurosci 108:1101–1106PubMedCrossRef Servatius RJ, Shors TJ (1994) Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav Neurosci 108:1101–1106PubMedCrossRef
go back to reference Shors TJ, Chua C, Falduto J (2001) Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21:6292–6297PubMed Shors TJ, Chua C, Falduto J (2001) Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21:6292–6297PubMed
go back to reference Shors TJ, Lewczyk C, Pacynski M, Mathew PR, Pickett J (1998) Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 9:419–423PubMedCrossRef Shors TJ, Lewczyk C, Pacynski M, Mathew PR, Pickett J (1998) Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 9:419–423PubMedCrossRef
go back to reference Shors TJ, Servatius RJ (1997) The contribution of stressor intensity, duration, and context to the stress-induced facilitation of associative learning. Neurobiol Learn Mem 68:92–96PubMedCrossRef Shors TJ, Servatius RJ (1997) The contribution of stressor intensity, duration, and context to the stress-induced facilitation of associative learning. Neurobiol Learn Mem 68:92–96PubMedCrossRef
go back to reference Sinha R, Lacadie C, Skudlarski P, Fulbright RK, Rounsaville BJ, Kosten TR, Wexler BE (2005) Neural activity associated with stress-induced cocaine craving: a functional magnetic resonance imaging study. Psychopharmacology (Berl) 183:171–180CrossRef Sinha R, Lacadie C, Skudlarski P, Fulbright RK, Rounsaville BJ, Kosten TR, Wexler BE (2005) Neural activity associated with stress-induced cocaine craving: a functional magnetic resonance imaging study. Psychopharmacology (Berl) 183:171–180CrossRef
go back to reference Smith A (1968) The Symbol-Digit Modalities Test: a neuropsychologic test for economic screening of learning and other cerebral disorders. Learn Disord 3:83–91 Smith A (1968) The Symbol-Digit Modalities Test: a neuropsychologic test for economic screening of learning and other cerebral disorders. Learn Disord 3:83–91
go back to reference VonDras DD, Powless MR, Olson AK, Wheeler D, Snudden AL (2005) Differential effects of everyday stress on the episodic memory test performances of young, mid-life, and older adults. Aging Ment Health 9:60–70PubMedCrossRef VonDras DD, Powless MR, Olson AK, Wheeler D, Snudden AL (2005) Differential effects of everyday stress on the episodic memory test performances of young, mid-life, and older adults. Aging Ment Health 9:60–70PubMedCrossRef
go back to reference Wilkinson GS (1993) Wide range achievement test 3—administration manual. Jastak Associates, Inc, Wilimington, DE Wilkinson GS (1993) Wide range achievement test 3—administration manual. Jastak Associates, Inc, Wilimington, DE
go back to reference Wolf OT, Schommer NC, Hellhammer DH, McEwen BS, Kirschbaum C (2001) The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 26:711–720PubMedCrossRef Wolf OT, Schommer NC, Hellhammer DH, McEwen BS, Kirschbaum C (2001) The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 26:711–720PubMedCrossRef
go back to reference Woods SP, Scott JC, Dawson MS, Morgan EE, Carey CL, Heaton RK, Grant I (2005) Construct validity of Hopkins Verbal Learning Test-Revised component process measures in an HIV-1 sample. Arch Clin Neuropsychol 20:1061–1071PubMedCrossRef Woods SP, Scott JC, Dawson MS, Morgan EE, Carey CL, Heaton RK, Grant I (2005) Construct validity of Hopkins Verbal Learning Test-Revised component process measures in an HIV-1 sample. Arch Clin Neuropsychol 20:1061–1071PubMedCrossRef
go back to reference Woon FL, Sood S, Hedges DW (2010) Hippocampal volume deficits associated with exposure to psychological trauma and posttraumatic stress disorder in adults: a meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 34:1181–1188PubMedCrossRef Woon FL, Sood S, Hedges DW (2010) Hippocampal volume deficits associated with exposure to psychological trauma and posttraumatic stress disorder in adults: a meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 34:1181–1188PubMedCrossRef
go back to reference Yehuda R, Harvey PD, Buchsbaum M, Tischler L, Schmeidler J (2007) Enhanced effects of cortisol administration on episodic and working memory in aging veterans with PTSD. Neuropsychopharmacology 32:2581–2591PubMedCrossRef Yehuda R, Harvey PD, Buchsbaum M, Tischler L, Schmeidler J (2007) Enhanced effects of cortisol administration on episodic and working memory in aging veterans with PTSD. Neuropsychopharmacology 32:2581–2591PubMedCrossRef
go back to reference Yusim A, Franklin L, Brooke S, Ajilore O, Sapolsky R (2000) Glucocorticoids exacerbate the deleterious effects of gp120 in hippocampal and cortical explants. J Neurochem 74:1000–1007PubMedCrossRef Yusim A, Franklin L, Brooke S, Ajilore O, Sapolsky R (2000) Glucocorticoids exacerbate the deleterious effects of gp120 in hippocampal and cortical explants. J Neurochem 74:1000–1007PubMedCrossRef
Metadata
Title
The association of perceived stress and verbal memory is greater in HIV-infected versus HIV-uninfected women
Authors
Leah H. Rubin
Judith A. Cook
Kathleen M. Weber
Mardge H. Cohen
Eileen Martin
Victor Valcour
Joel Milam
Kathryn Anastos
Mary A. Young
Christine Alden
Deborah R. Gustafson
Pauline M. Maki
Publication date
01-08-2015
Publisher
Springer US
Published in
Journal of NeuroVirology / Issue 4/2015
Print ISSN: 1355-0284
Electronic ISSN: 1538-2443
DOI
https://doi.org/10.1007/s13365-015-0331-5

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