Skip to main content

Advertisement

Log in

Translational spatial task and its relationship to HIV-associated neurocognitive disorders and apolipoprotein E in HIV-seropositive women

  • Published:
Journal of NeuroVirology Aims and scope Submit manuscript

Abstract

HIV-associated neurocognitive disorders (HAND) continue to be a neurological complication of HIV infection in the era of combined antiretroviral therapy. Hippocampal neurodegeneration and dysfunction occurs as a result of HIV infection, but few studies to date have assesses spatial learning and memory function in patients with HAND. We used the Memory Island (MI) test to study the effects of HIV infection, apolipoprotein E (ApoE) allele status, and cerebral spinal fluid (CSF) ApoE protein levels on spatial learning and memory in our cohort of Hispanic women. The MI test is a virtual reality-based computer program that tests spatial learning and memory and was designed to resemble the Morris Water Maze test of hippocampal function widely used in rodent studies. In the current study, HIV-seropositive women (n = 20) and controls (n = 16) were evaluated with neuropsychological (NP) tests, the MI test, ApoE, and CSF ApoE assays. On the MI, the HIV-seropositive group showed significant reduced learning and delayed memory performance compared with HIV-seronegative controls. When stratified by cognitive performance on NP tests, the HIV-seropositive, cognitively impaired group performed worse than HIV-seronegative controls in ability to learn and in the delayed memory trial. Interestingly, differences were observed in the results obtained by the NP tests and the MI test for ε4 carriers and noncarriers: NP tests showed effects of the ε4 allele in HIV-seronegative women but not HIV-seropositive ones, whereas the converse was true for the MI test. Our findings suggest that the MI test is sensitive in detecting spatial deficits in HIV-seropositive women and that these deficits may arise relatively early in the course of HAND.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acevedo SF, Piper BJ, Craytor MJ, Benice TS, Raber J (2010) Apolipoprotein E4 and sex affect neurobehavioral performance in primary school children. Pediatr Res 67:293–299

    Article  PubMed  CAS  Google Scholar 

  • Alexander DM, Williams LM, Gatt JM, Dobson-Stone C, Kuan SA, Todd EG, Schofield PR, Cooper NJ, Gordon E (2007) The contribution of apolipoprotein E alleles on cognitive performance and dynamic neural activity over six decades. Biol Psychol 75:229–238

    Article  PubMed  CAS  Google Scholar 

  • Al-Khindi T, Zakzanis KK, van Gorp WG (2011) Does antiretroviral therapy improve HIV-associated cognitive impairment? A quantitative review of the literature. J Int Neuropsychol Soc 17:956–969

    Google Scholar 

  • American Academy of Neurology AIDS Task Force (1991) Nomenclature and research case definitions for neurologic manifestations of human immunodeficiency virus-type 1 (HIV-1) infection. Report of a Working Group of the American Academy of Neurology AIDS Task Force. Neurology 41:778–785

    Article  Google Scholar 

  • American Academy of Neurology AIDS Task Force (1996) Clinical confirmation of the American Academy of Neurology algorithm for HIV-1-associated cognitive/motor disorder. The Dana Consortium on Therapy for HIV Dementia and Related Cognitive Disorders. Neurology 47:1247–1253

    Article  Google Scholar 

  • Andres MA, Feger U, Nath A, Munsaka S, Jiang CS, Chang L (2011) APOE epsilon 4 allele and CSF APOE on cognition in HIV-infected subjects. J Neuroimmune Pharmacol 6:389–398

    Article  PubMed  Google Scholar 

  • Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslen M, Grant I, Heaton RK, Joseph J, Marder K, Marra CM, McArthur JC, Nunn M, Price RW, Pulliam L, Robertson KR, Sacktor N, Valcour V, Wojna VE (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799

    Article  PubMed  CAS  Google Scholar 

  • Archibald SL, Masliah E, Fennema-Notestine C, Marcotte TD, Ellis RJ, McCutchan JA, Heaton RK, Grant I, Mallory M, Miller A, Jernigan TL (2004) Correlation of in vivo neuroimaging abnormalities with postmortem human immunodeficiency virus encephalitis and dendritic loss. Arch Neurol 61:369–376

    Article  PubMed  Google Scholar 

  • Ayala-Feliciano M, Pons-Valerio JJ, Pons-Madera J, Acevedo SF (2011) The relationship between visuospatial memory and coping strategies in breast cancer survivors. Breast Can Basic Clin Res 5:117–130

    Google Scholar 

  • Bu G (2009) Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 10:333–344

    Article  PubMed  CAS  Google Scholar 

  • Burgess N (2008) Spatial cognition and the brain. Ann N Y Acad Sci 1124:77–97

    Article  PubMed  Google Scholar 

  • Burt TD, Agan BK, Marconi VC, He W, Kulkarni H, Mold JE, Cavrois M, Huang Y, Mahley RW, Dolan MJ, McCune JM, Ahuja SK (2008) Apolipoprotein (apo) E4 enhances HIV-1 cell entry in vitro, and the APOE epsilon4/epsilon4 genotype accelerates HIV disease progression. Proc Natl Acad Sci U S A 105:8718–8723

    Article  PubMed  CAS  Google Scholar 

  • Castelo JM, Sherman SJ, Courtney MG, Melrose RJ, Stern CE (2006) Altered hippocampal-prefrontal activation in HIV patients during episodic memory encoding. Neurology 66:1688–1695

    Article  PubMed  CAS  Google Scholar 

  • Cohen RA, Gongvatana A (2010) The persistence of HIV-associated neurocognitive dysfunction and the effects of comorbidities. Neurology 75:2052–2053

    Article  PubMed  Google Scholar 

  • Corder EH, Robertson K, Lannfelt L, Bogdanovic N, Eggertsen G, Wilkins J, Hall C (1998) HIV-infected subjects with the E4 allele for APOE have excess dementia and peripheral neuropathy. Nat Med 4:1182–1184

    Article  PubMed  CAS  Google Scholar 

  • D'Hooge R, De Deyn PP (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36:60–90

    Article  PubMed  Google Scholar 

  • D'Hooge R, Franck F, Mucke L, De Deyn PP (1999) Age-related behavioural deficits in transgenic mice expressing the HIV-1 coat protein gp120. Eur J Neurosci 11:4398–4402

    Article  PubMed  Google Scholar 

  • Dunlop O, Goplen AK, Liestol K, Myrvang B, Rootwelt H, Christophersen B, Kvittingen EA, Maehlen J (1997) HIV dementia and apolipoprotein E. Acta Neurol Scand 95:315–318

    Article  PubMed  CAS  Google Scholar 

  • Fitting S, Booze RM, Mactutus CF (2008) Neonatal intrahippocampal injection of the HIV-1 proteins gp120 and Tat: differential effects on behavior and the relationship to stereological hippocampal measures. Brain Res 1232:139–154

    Article  PubMed  CAS  Google Scholar 

  • Fukuyama R, Mizuno T, Mori S, Yanagisawa K, Nakajima K, Fushiki S (2000) Age-dependent decline in the apolipoprotein E level in cerebrospinal fluid from control subjects and its increase in cerebrospinal fluid from patients with Alzheimer's disease. Eur Neurol 43:161–169

    Article  PubMed  CAS  Google Scholar 

  • Glowa JR, Panlilio LV, Brenneman DE, Gozes I, Fridkin M, Hill JM (1992) Learning impairment following intracerebral administration of the HIV envelope protein gp120 or a VIP antagonist. Brain Res 570:49–53

    Article  PubMed  CAS  Google Scholar 

  • Griffin WC, Middaugh D, Cook JE, Tyor WR (2004) The severe combined immunodeficient (SCID) mouse model of human immunodeficiency virus encephalitis: deficits in cognitive function. J Neurovirol 10:109–115

    Article  PubMed  Google Scholar 

  • Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 75:2087–2096

    Article  PubMed  Google Scholar 

  • 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 17:3–16

    Google Scholar 

  • Herz J, Beffert U (2000) Apolipoprotein E receptors: linking brain development and Alzheimer's disease. Nat Rev Neurosci 1:51–58

    Article  PubMed  CAS  Google Scholar 

  • Joska JA, Combrinck M, Valcour VG, Hoare J, Leisegang F, Mahne AC, Myer L, Stein DJ (2010) Association between apolipoprotein E4 genotype and human immunodeficiency virus-associated dementia in younger adults starting antiretroviral therapy in South Africa. J Neurovirol 16:377–383

    Article  PubMed  CAS  Google Scholar 

  • Keblesh JP, Dou H, Gendelman HE, Xiong H (2009) 4-Aminopyridine improves spatial memory in a murine model of HIV-1 encephalitis. J Neuroimmune Pharmacol 4:317–327

    Article  PubMed  Google Scholar 

  • Kim HJ, Martemyanov KA, Thayer SA (2008) Human immunodeficiency virus protein Tat induces synapse loss via a reversible process that is distinct from cell death. J Neurosci 28:12604–12613

    Article  PubMed  CAS  Google Scholar 

  • Krikorian R, Wrobel AJ, Meinecke C, Liang WM, Kay J (1990) Cognitive deficits associated with human immunodeficiency virus encephalopathy. J Neuropsychiatry Clin Neurosci 2:256–260

    PubMed  CAS  Google Scholar 

  • Lashomb AL, Vigorito M, Chang SL (2009) Further characterization of the spatial learning deficit in the human immunodeficiency virus-1 transgenic rat. J Neurovirol 15:14–24

    Article  PubMed  CAS  Google Scholar 

  • Lee MH, Wang T, Jang MH, Steiner J, Haughey N, Ming GL, Song H, Nath A, Venkatesan A (2011) Rescue of adult hippocampal neurogenesis in a mouse model of HIV neurologic disease. Neurobiol Dis 41:678–687

    Article  PubMed  CAS  Google Scholar 

  • Letendre SL, Ellis RJ, Ances BM, McCutchan JA (2010) Neurologic complications of HIV disease and their treatment. Top HIV Med 18:45–55

    PubMed  Google Scholar 

  • Li ST, Matsushita M, Moriwaki A, Saheki Y, Lu YF, Tomizawa K, Wu HY, Terada H, Matsui H (2004) HIV-1 Tat inhibits long-term potentiation and attenuates spatial learning [corrected]. Ann Neurol 55:362–371

    Article  PubMed  CAS  Google Scholar 

  • Luo X, Carlson KA, Wojna V, Mayo R, Biskup TM, Stoner J, Anderson J, Gendelman HE, Melendez LM (2003) Macrophage proteomic fingerprinting predicts HIV-1-associated cognitive impairment. Neurology 60:1931–1937

    Article  PubMed  CAS  Google Scholar 

  • Maki PM, Martin-Thormeyer E (2009) HIV, cognition and women. Neuropsychol Rev 19:204–214

    Article  PubMed  Google Scholar 

  • Maruff P, Malone V, McArthur-Jackson C, Mulhall B, Benson E, Currie J (1995) Abnormalities of visual spatial attention in HIV infection and the HIV-associated dementia complex. J Neuropsychiatry Clin Neurosci 7:325–333

    PubMed  CAS  Google Scholar 

  • McArthur JC (2004) HIV dementia: an evolving disease. J Neuroimmunol 157:3–10

    Article  PubMed  CAS  Google Scholar 

  • McArthur JC, Brew BJ (2010) HIV-associated neurocognitive disorders: is there a hidden epidemic? AIDS 24:1367–1370

    Article  PubMed  Google Scholar 

  • McArthur JC, Steiner J, Sacktor N, Nath A (2010) Human immunodeficiency virus-associated neurocognitive disorders: mind the gap. Ann Neurol 67:699–714

    Article  PubMed  CAS  Google Scholar 

  • Mishkin M, Appenzeller T (1987) The anatomy of memory. Sci Am 256:80–89

    Article  PubMed  CAS  Google Scholar 

  • Mondadori CR, de Quervain DJ, Buchmann A, Mustovic H, Wollmer MA, Schmidt CF, Boesiger P, Hock C, Nitsch RM, Papassotiropoulos A, Henke K (2007) Better memory and neural efficiency in young apolipoprotein E epsilon4 carriers. Cereb Cortex 17:1934–1947

    Article  PubMed  Google Scholar 

  • Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47–60

    Article  PubMed  CAS  Google Scholar 

  • Newman MF, Croughwell ND, Blumenthal JA, Lowry E, White WD, Spillane W, Davis RD, Glower DD, Smith LR, Mahanna EP (1995) Predictors of cognitive decline after cardiac operation. Ann Thorac Surg 59:1326–1330

    Article  PubMed  CAS  Google Scholar 

  • Olesen PJ, Schendan HE, Amick MM, Cronin-Golomb A (2007) HIV infection affects parietal-dependent spatial cognition: evidence from mental rotation and hierarchical pattern perception. Behav Neurosci 121:1163–1173

    Article  PubMed  Google Scholar 

  • Payami H, Zareparsi S, Montee KR, Sexton GJ, Kaye JA, Bird TD, Yu CE, Wijsman EM, Heston LL, Litt M, Schellenberg GD (1996) Gender difference in apolipoprotein E-associated risk for familial Alzheimer disease: a possible clue to the higher incidence of Alzheimer disease in women. Am J Hum Genet 58:803–811

    PubMed  CAS  Google Scholar 

  • Piper BJ, Acevedo SF, Craytor MJ, Murray PW, Raber J (2010) The use and validation of the spatial navigation Memory Island test in primary school children. Behav Brain Res 210:257–262

    Article  PubMed  Google Scholar 

  • Pomara N, Belzer K, Sidtis JJ (2008) Deleterious CNS effects of the APOE epsilon4 allele in individuals with HIV-1 infection may be age-dependent. Proc Natl Acad Sci U S A 105:E65, author reply E67–68

    Article  PubMed  CAS  Google Scholar 

  • Raber J (2008) AR, apoE, and cognitive function. Horm Behav 53:706–715

    Article  PubMed  CAS  Google Scholar 

  • Raber J, Wong D, Yu GQ, Buttini M, Mahley RW, Pitas RE, Mucke L (2000) Apolipoprotein E and cognitive performance. Nature 404:352–354

    Article  PubMed  CAS  Google Scholar 

  • Rackstraw S (2011) HIV-related neurocognitive impairment—a review. Psychol Health Med 16:548–563

    Article  PubMed  Google Scholar 

  • Ragin AB, Storey P, Cohen BA, Edelman RR, Epstein LG (2004) Disease burden in HIV-associated cognitive impairment: a study of whole-brain imaging measures. Neurology 63:2293–2297

    Article  PubMed  CAS  Google Scholar 

  • Rizk-Jackson AM, Acevedo SF, Inman D, Howieson D, Benice TS, Raber J (2006) Effects of sex on object recognition and spatial navigation in humans. Behav Brain Res 173:181–190

    Article  PubMed  Google Scholar 

  • Rizk-Jackson A, Robertson J, Raber J (2008) Tfm-AR modulates the effects of ApoE4 on cognition. J Neurochem 105:63–67

    Article  PubMed  CAS  Google Scholar 

  • Rohit M, Levine A, Hinkin C, Abramyan S, Saxton E, Valdes-Sueiras M, Singer E (2007) Education correction using years in school or reading grade-level equivalent? Comparing the accuracy of two methods in diagnosing HIV-associated neurocognitive impairment. J Int Neuropsychol Soc 13:462–470

    Article  PubMed  Google Scholar 

  • Sa MJ, Madeira MD, Ruela C, Volk B, Mota-Miranda A, Paula-Barbosa MM (2004) Dendritic changes in the hippocampal formation of AIDS patients: a quantitative Golgi study. Acta Neuropathol 107:97–110

    Article  PubMed  CAS  Google Scholar 

  • Sacktor N, McDermott MP, Marder K, Schifitto G, Selnes OA, McArthur JC, Stern Y, Albert S, Palumbo D, Kieburtz K, De Marcaida JA, Cohen B, Epstein L (2002) HIV-associated cognitive impairment before and after the advent of combination therapy. J Neurovirol 8:136–142

    Article  PubMed  Google Scholar 

  • Sanchez-Alavez M, Criado J, Gomez-Chavarin M, Jimenez-Anguiano A, Navarro L, Diaz-Ruiz O, Galicia O, Sanchez-Narvaez F, Murillo-Rodriguez E, Henriksen SJ, Elder JH, Prospero-Garcia O (2000) HIV- and FIV-derived gp120 alter spatial memory, LTP, and sleep in rats. Neurobiol Dis 7:384–394

    Article  PubMed  CAS  Google Scholar 

  • Schouten J, Cinque P, Gisslen M, Reiss P, Portegies P (2011) HIV-1 infection and cognitive impairment in the cART era: a review. AIDS 25:561–575

    Article  PubMed  Google Scholar 

  • Selnes OA (2005) Memory loss in persons with HIV/AIDS: assessment and strategies for coping. AIDS Read 15(289–92):294

    Google Scholar 

  • Shi J, Zhao CB, Vollmer TL, Tyry TM, Kuniyoshi SM (2008) APOE epsilon 4 allele is associated with cognitive impairment in patients with multiple sclerosis. Neurology 70:185–190

    Article  PubMed  CAS  Google Scholar 

  • Tang H, Lu D, Pan R, Qin X, Xiong H, Dong J (2009) Curcumin improves spatial memory impairment induced by human immunodeficiency virus type 1 glycoprotein 120 V3 loop peptide in rats. Life Sci 85:1–10

    Article  PubMed  CAS  Google Scholar 

  • Toro-Nieves DM, Rodriguez Y, Plaud M, Ciborowski P, Duan F, Perez Laspiur J, Wojna V, Melendez LM (2009) Proteomic analyses of monocyte-derived macrophages infected with human immunodeficiency virus type 1 primary isolates from Hispanic women with and without cognitive impairment. J Neurovirol 15:36–50

    Article  PubMed  CAS  Google Scholar 

  • Valcour V, Shikuma C, Shiramizu B, Watters M, Poff P, Selnes O, Holck P, Grove J, Sacktor N (2004a) Higher frequency of dementia in older HIV-1 individuals: the Hawaii Aging with HIV-1 Cohort. Neurology 63:822–827

    Article  PubMed  CAS  Google Scholar 

  • Valcour V, Shikuma C, Shiramizu B, Watters M, Poff P, Selnes OA, Grove J, Liu Y, Abdul-Majid KB, Gartner S, Sacktor N (2004b) Age, apolipoprotein E4, and the risk of HIV dementia: the Hawaii Aging with HIV Cohort. J Neuroimmunol 157:197–202

    Article  PubMed  CAS  Google Scholar 

  • Vance JE, Hayashi H (2010) Formation and function of apolipoprotein E-containing lipoproteins in the nervous system. Biochim Biophys Acta 1801:806–818

    Article  PubMed  CAS  Google Scholar 

  • Velázquez I, Plaud M, Wojna V, Skolasky R, Laspiur JP, Meléndez LM (2009) Antioxidant enzyme dysfunction in monocytes and CSF of Hispanic women with HIV-associated cognitive impairment. J Neuroimmunol 206:106–111

    Article  PubMed  Google Scholar 

  • Vigorito M, LaShomb AL, Chang SL (2007) Spatial learning and memory in HIV-1 transgenic rats. J Neuroimmune Pharmacol 2:319–328

    Article  PubMed  Google Scholar 

  • Wenham PR, Price WH, Blandell G (1991) Apolipoprotein E genotyping by one-stage PCR. Lancet 337:1158–1159

    Article  PubMed  CAS  Google Scholar 

  • Wiley CA, Soontornniyomkij V, Radhakrishnan L, Masliah E, Mellors J, Hermann SA, Dailey P, Achim CL (1998) Distribution of brain HIV load in AIDS. Brain Pathol 8:277–284

    Article  PubMed  CAS  Google Scholar 

  • Wojna V, Skolasky RL, Hechavarria R, Mayo R, Selnes O, McArthur JC, Melendez LM, Maldonado E, Zorrilla CD, Garcia H, Kraiselburd E, Nath A (2006) Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment. J Neurovirol 12:356–364

    Article  PubMed  Google Scholar 

  • Wojna V, Robles L, Skolasky RL, Mayo R, Selnes O, de la Torre T, Maldonado E, Nath A, Melendez LM, Lasalde-Dominicci J (2007a) Associations of cigarette smoking with viral immune and cognitive function in human immunodeficiency virus-seropositive women. J Neurovirol 13:561–568

    Article  PubMed  CAS  Google Scholar 

  • Wojna V, Skolasky RL, McArthur JC, Maldonado E, Hechavarria R, Mayo R, Selnes O, Ginebra T, de la Torre T, Garcia H, Kraiselburd E, Melendez-Guerrero LM, Zorrilla CD, Nath A (2007b) Spanish validation of the HIV Dementia Scale in Women. AIDS Patient Care STDS 21:930–941

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Bae M, Tovar-y-Romo LB, Patel N, Bandaru VV, Pomerantz D, Steiner JP, Haughey NJ (2011) The human immunodeficiency virus coat protein gp120 promotes forward trafficking and surface clustering of NMDA receptors in membrane microdomains. J Neurosci 31:17074–17090

    Article  PubMed  CAS  Google Scholar 

  • Zink WE, Anderson E, Boyle J, Lynette H, Rodriguez JS, Xiong H, Gendelman HE, Persidsky Y (2002) Impaired spatial cognition and synaptic potentiation in a murine model of human immunodeficiency virus type 1 encephalitis. J Neurosci 22:2096–2105

    PubMed  CAS  Google Scholar 

  • Zola SM, Squire LR, Teng E, Stefanacci L, Buffalo EA, Clark RE (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20:451–463

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I would like to thank Madeline Collazo for helping with genotyping. The study was funded by National Center for Research Resources (NCRR) grant 1U54RR026139-01A1 and the National Institute on Minority Health and Health Disparities 8U54MD007587 to the University of Puerto Rico-Medical Science Campus, and National Institute of Mental Health (NIMH) Center for Novel Therapeutics of HIV-associated Cognitive Disorders Pilot Project Grant G12 RR003050 to the John Hopkins University. The study was partially supported by National Institute of Neurological Disorders and Stroke (NINDS) grants S11NS46278 and U54NS43011 (SNRP). The content of this publication is solely the responsibility of the authors and does not necessarily represent the official views of NCRR, NIMHD, NIMH, or NINDS. Thanks to Dr. Carlos Pardo at John Hopkins University for the control CSF samples. Thanks to Dr. Jacob Raber at Oregon Health & Science University for permission to use the Memory Island and serving as an excellent mentor. We also appreciate the contribution from Dr. Raul Mayo whom conducted neuropsychological testing of cohort participates and Dr. Avindra Nath for his contribution in the development of the cohort and continuous collaboration with the SNRP. We acknowledge the support of Tirtsa Porrata-Doria and the Molecular Biology Core Lab (grant RR003050). Special thanks go to Robert Ritchie of the RCMI Publications Office (G12 RR003050).

Declaration of interest

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Valerie Wojna.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morales, D., Acevedo, S.F., Skolasky, R.L. et al. Translational spatial task and its relationship to HIV-associated neurocognitive disorders and apolipoprotein E in HIV-seropositive women. J. Neurovirol. 18, 488–502 (2012). https://doi.org/10.1007/s13365-012-0128-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13365-012-0128-8

Keywords

Navigation