Skip to main content

Advertisement

SpringerLink
Log in

Brain structural correlates of trajectories to cognitive impairment in men with and without HIV disease

  • ORIGINAL RESEARCH
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

There are distinct trajectories to cognitive impairment among participants in the Multicenter AIDS Cohort Study (MACS). Here we analyzed the relationship between regional brain volumes and the individual trajectories to impairment in a subsample (n = 302) of the cohort. 302 (167 HIV-infected; mean age = 55.7 yrs.; mean education: 16.2 yrs.) of the men enrolled in the MACS MRI study contributed data to this analysis. We used voxel-based morphometry (VBM) to segment the brain images to analyze gray and white matter volume at the voxel-level. A Mixed Membership Trajectory Model had previously identified three distinct profiles, and each study participant had a membership weight for each of these three trajectories. We estimated VBM model parameters for 100 imputations, manually performed the post-hoc contrasts, and pooled the results. We examined the associations between brain volume at the voxel level and the MMTM membership weights for two profiles: one considered “unhealthy” and the other considered “Premature aging.” The unhealthy profile was linked to the volume of the posterior cingulate gyrus/precuneus, the inferior frontal cortex, and the insula, whereas the premature aging profile was independently associated with the integrity of a portion of the precuneus. Trajectories to cognitive impairment are the result, in part, of atrophy in cortical regions linked to normal and pathological aging. These data suggest the possibility of predicting cognitive morbidity based on patterns of CNS atrophy.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ances, B. M., & Hammoud, D. A. (2014). Neuroimaging of HIV-associated neurocognitive disorders (HAND). Current Opinion in HIV and AIDS, 9(6), 545–551. https://doi.org/10.1097/COH.0000000000000112.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ances, B. M., Ortega, M., Vaida, F., Heaps, J., & Paul, R. (2012). Independent effects of HIV, aging, and HAART on brain volumetric measures. Journal of Acquired Immune Deficiency Syndromes, 59(5), 469–477. https://doi.org/10.1097/QAI.0b013e318249db17.

    Article  PubMed  Google Scholar 

  • Antinori, A., Arendt, G., Becker, J. T., Brew, B. J., Byrd, D. A., Cherner, M., et al. (2007). Updated research nosology for HIV-associated neurocognitive disorders. Neurology, 69(18), 1789–1799.

    Article  CAS  Google Scholar 

  • Bailly, M., Destrieux, C., Hommet, C., Mondon, K., Cottier, J. P., Beaufils, E., et al. (2015). Precuneus and cingulate cortex atrophy and Hypometabolism in patients with Alzheimer's disease and mild cognitive impairment: MRI and (18)F-FDG PET quantitative analysis using FreeSurfer. BioMed Research International, 2015, 583931. https://doi.org/10.1155/2015/583931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker, J. T., Maruca, V., Kingsley, L. A., Sanders, J. M., Alger, J. R., Barker, P. B., et al. (2011). Factors affecting brain structure in men with HIV disease in the post-HAART era. Neuroradiology, 54, 113–121. https://doi.org/10.1007/s00234-011-0854-2.

    Article  PubMed  PubMed Central  Google Scholar 

  • Becker, J. T., Bajo, R., Fabrizio, M., Sudre, G., Cuesta, P., Aizenstein, H. J., et al. (2012a). Functional connectivity measured with magnetoencephalography identifies persons with HIV disease. Brain Imaging and Behavior, 6(3), 366–373. https://doi.org/10.1007/s11682-012-9149-4.

    Article  PubMed  PubMed Central  Google Scholar 

  • Becker, J. T., Cuesta, P., Fabrizio, M., Sudre, G., Vergis, E. N., Douaihy, A., et al. (2012b). Brain structural and functional recovery following initiation of combination antiretroviral therapy. Journal of Neurovirology, 18(5), 423–427. https://doi.org/10.1007/s13365-012-0115-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardenas, V. A., Meyerhoff, D. J., Studholme, C., Kornak, J., Rothlind, J., Lampiris, H., et al. (2009). Evidence for ongoing brain injury in human immunodeficiency virus-positive patients treated with antiretroviral therapy. Journal of Neurovirology, 15(4), 324–333. https://doi.org/10.1080/13550280902973960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang, L., Ernst, T., Ames, N., Walot, I., Jovicich, J., DeSilva, M., et al. (2003). Persistent brain abnormalities in antiretroviral-naive HIV patients 3 months after HAART. Antiviral Therapy, 8(1), 17–26.

    CAS  PubMed  Google Scholar 

  • Cohen, R. A., & Gongvatana, A. (2011). The persistence of HIV-associated neurocognitive dysfunction and the effects of comorbidities. Neurology, 75(23), 2052–2053. https://doi.org/10.1212/WNL.0b013e318200d833.

    Article  Google Scholar 

  • Cohen, R. A., Harezlak, J., Gongvatana, A., Buchthal, S., Schifitto, G., Clark, U., et al. (2010). Cerebral metabolite abnormalities in human immunodeficiency virus are associated with cortical and subcortical volumes. Journal of Neurovirology, 16(6), 435–444. https://doi.org/10.3109/13550284.2010.520817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connor, J. T. (2006). Multivariate Mixture Models to Describe Longitudinal Patterns of Frailty in American Seniors. Pittsburgh, PA: Carnegie Mellon University, ProQuest, UMI Dissertations Publishing. 3275170.

  • Cysique, L. A., Moffat, K., Moore, D. M., Lane, T. A., Davies, N. W., Carr, A., et al. (2013). HIV, vascular and aging injuries in the brain of clinically stable HIV-infected adults: A (1)H MRS study. PLoS One, 8(4), e61738. https://doi.org/10.1371/journal.pone.0061738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ernst, T., Jiang, C. S., Nakama, H., Buchthal, S., & Chang, L. (2010). Lower brain glutamate is associated with cognitive deficits in HIV patients: A new mechanism for HIV-associated neurocognitive disorder. Journal of Magnetic Resonance Imaging, 32(5), 1045–1053. https://doi.org/10.1002/jmri.22366.

    Article  PubMed  Google Scholar 

  • Erosheva, E. A. (2005). Comparing latent structures of the grade of membership, Rasch, and latent class models. Psychometrika, 70(4), 619–628. https://doi.org/10.1007/s11336-001-0899-y.

    Article  Google Scholar 

  • Erosheva, E. A., Fienberg, S. E., & Joutard, C. (2007). Describing disability through individual-level mixture models for multivariate binary data. Ann. Appl. Stat., 1(2), 346–384.

    Article  Google Scholar 

  • Fennema-Notestine, C., Ellis, R. J., Archibald, S. L., Jernigan, T. L., Letendre, S. L., Notestine, R. J., et al. (2013). Increases in brain white matter abnormalities and subcortical gray matter are linked to CD4 recovery in HIV infection. Journal of Neurovirology, 19(4), 393–401. https://doi.org/10.1007/s13365-013-0185-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friston, K. J., Ashburner, J., Kiebel, S. J., Nichols, T. E., & Penny, W. D. (Eds.). (2007). Statistical Parametric Mapping: The Analysis of Functional Brain Images: Academic Press.

  • Harezlak, J., Buchthal, S., Taylor, M., Schifitto, G., Zhong, J., Daar, E., et al. (2011). Persistence of HIV-associated cognitive impairment, inflammation, and neuronal injury in era of highly active antiretroviral treatment. AIDS, 25(5), 625–633. https://doi.org/10.1097/QAD.0b013e3283427da7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jernigan, T. L., Archibald, S. L., Fennema-Notestine, C., Taylor, M. J., Theilmann, R. J., Julaton, M. D., et al. (2011). Clinical factors related to brain structure in HIV: The CHARTER study. Journal of Neurovirology, 17(3), 248–257. https://doi.org/10.1007/s13365-011-0032-7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones, B. F., Barnes, J., Uylings, H. B., Fox, N. C., Frost, C., Witter, M. P., & Scheltens, P. (2006). Differential regional atrophy of the cingulate gyrus in Alzheimer disease: A volumetric MRI study. Cerebral Cortex, 16(12), 1701–1708. https://doi.org/10.1093/cercor/bhj105.

    Article  PubMed  Google Scholar 

  • Kallianpur, K. J., Shikuma, C., Kirk, G. R., Shiramizu, B., Valcour, V., Chow, D., et al. (2013). Peripheral blood HIV DNA is associated with atrophy of cerebellar and subcortical gray matter. Neurology, 80(19), 1792–1799. https://doi.org/10.1212/WNL.0b013e318291903f.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karas, G., Scheltens, P., Rombouts, S., van Schijndel, R., Klein, M., Jones, B., et al. (2007). Precuneus atrophy in early-onset Alzheimer's disease: A morphometric structural MRI study. Neuroradiology, 49(12), 967–976.

    Article  Google Scholar 

  • Kaslow, R. A., Ostrow, D. G., Detels, R., Phair, J. P., Polk, B. F., & Rinaldo, C. R. (1987). The multicenter AIDS cohort study (MACS): Rationale, organization, and selected characteristics of the participants. American Journal of Epidemiology, 126, 310–318.

    Article  CAS  Google Scholar 

  • Kuper, M., Rabe, K., Esser, S., Gizewski, E. R., Husstedt, I. W., Maschke, M., & Obermann, M. (2011). Structural gray and white matter changes in patients with HIV. Journal of Neurology, 258, 1066–1075. https://doi.org/10.1007/s00415-010-5883-y.

    Article  PubMed  Google Scholar 

  • Lake, J. E., Popov, M., Post, W. S., Palella, F. J., Sacktor, N., Miller, E. N., et al. (2017). Visceral fat is associated with brain structure independent of human immunodeficiency virus infection status. Journal of Neurovirology, 23(3), 385–393. https://doi.org/10.1007/s13365-016-0507-7.

    Article  CAS  PubMed  Google Scholar 

  • Lepore, N., Brun, C. A., Chou, Y. Y., Chiang, M. C., Dutton, R. A., Hayashi, K. M., et al. (2008). Generalized tensor-based morphometry of HIV/AIDS usingmultivariate statistics on strain matrices and their application to HIV/AIDS. IEEE Transactions on Medical Imaging, Special Issue on Computational Neuroanatomy, 27(1), 129–141.

    CAS  Google Scholar 

  • Manji, H., Jager, H. R., & Winston, A. (2013). HIV, dementia and antiretroviral drugs: 30 years of an epidemic. Journal of Neurology, Neurosurgery, and Psychiatry, 84(10), 1126–1137. https://doi.org/10.1136/jnnp-2012-304022.

    Article  PubMed  Google Scholar 

  • Manrique-Vallier, D. (2014). Mixed membership trajectory models. In E. Airoldi, D. Blei, E. E., & F. S. (Eds.), Handbook of mixed membership models and their applications (pp. 173–188). New York: Chapman-Hall.

  • Masters, M. C., & Ances, B. M. (2014). Role of neuroimaging in HIV-associated neurocognitive disorders. Seminars in Neurology, 34(1), 89–102. https://doi.org/10.1055/s-0034-1372346.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller, E. N., Selnes, O. A., & McArthur, M. B. (1990). Neuropsychological test performance in HIV1-infected homosexual men: The multicenter AIDS cohort study (MACS). Neurology, 40, 197–203.

    Article  CAS  Google Scholar 

  • Molsberry, S. A., Lecci, F., Kingsley, L., Junker, B., Reynolds, S., Goodkin, K., et al. (2015). Mixed membership trajectory models of cognitive impairment in the multicenter AIDS cohort study. AIDS, 29(6), 713–721. https://doi.org/10.1097/QAD.0000000000000561.

    Article  PubMed  PubMed Central  Google Scholar 

  • O'Connor, E. E., Jaillard, A., Renard, F., & Zeffiro, T. A. (2017a). Reliability of white matter microstructural changes in HIV infection: Meta-analysis and confirmation. AJNR. American Journal of Neuroradiology, 38(8), 1510–1519. https://doi.org/10.3174/ajnr.A5229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O'Connor, E. E., Zeffiro, T. A., & Zeffiro, T. A. (2017b). Brain structural changes following HIV infection: Meta-analysis. AJNR. American Journal of Neuroradiology, 39, 54–62. https://doi.org/10.3174/ajnr.A5432.

    Article  PubMed  Google Scholar 

  • Paul, R., Cohen, R., Navia, B., & Tashima, K. (2002). Relationships between cognition and structural neuroimaging findings in adults with human immunodeficiency virus type-1. Neuroscience and Behavioral Reviews, 26, 353–359.

    Article  Google Scholar 

  • Ragin, A. B., Du, H., Ochs, R., Wu, Y., Sammet, C. L., Shoukry, A., & Epstein, L. G. (2012). Structural brain alterations can be detected early in HIV infection. Neurology, 79(24), 2328–2334. https://doi.org/10.1212/WNL.0b013e318278b5b4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosen, B. R., Huang, S. Y., & Stufflebeam, S. M. (2015). Pushing the limits of human neuroimaging. JAMA, 314(10), 993–994. https://doi.org/10.1001/jama.2015.10229.

    Article  CAS  PubMed  Google Scholar 

  • Rubin, D. B. (1986). Multiple imputation for nonresponse in surveys: John Wiley & Sons.

  • Sacktor, N., McDermott, M. P., Marder, K., Schifitto, G., Selnes, O. A., McArthur, J. C., et al. (2002). HIV-associated cognitive impairment before and after the advent of combination therapy. Journal of Neurovirology, 8, 136–142.

    Article  Google Scholar 

  • Sanford, R., Fernandez Cruz, A. L., Scott, S. C., Mayo, N. E., Fellows, L. K., Ances, B. M., & Collins, D. L. (2017). Regionally specific brain volumetric and cortical thickness changes in HIV-infected patients in the HAART era. Journal of Acquired Immune Deficiency Syndromes, 74(5), 563–570. https://doi.org/10.1097/QAI.0000000000001294.

    Article  PubMed  Google Scholar 

  • Saylor, D., Dickens, A. M., Sacktor, N., Haughey, N., Slusher, B., Pletnikov, M., et al. (2016). HIV-associated neurocognitive disorder--pathogenesis and prospects for treatment. Nature Reviews. Neurology, 12(4), 234–248. https://doi.org/10.1038/nrneurol.2016.27.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sled, J. G., Zijdenbos, A. P., & Evans, A. C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical Imaging, 17(1), 87–97. https://doi.org/10.1109/42.668698.

    Article  CAS  PubMed  Google Scholar 

  • Spies, G., Ahmed-Leitao, F., Fennema-Notestine, C., Cherner, M., & Seedat, S. (2016). Effects of HIV and childhood trauma on brain morphometry and neurocognitive function. Journal of Neurovirology, 22(2), 149–158. https://doi.org/10.1007/s13365-015-0379-2.

    Article  PubMed  Google Scholar 

  • Thames, A. D., Kuhn, T. P., Williamson, T. J., Jones, J. D., Mahmood, Z., & Hammond, A. (2017). Marijuana effects on changes in brain structure and cognitive function among HIV+ and HIV- adults. Drug and Alcohol Dependence, 170, 120–127. https://doi.org/10.1016/j.drugalcdep.2016.11.007.

    Article  CAS  PubMed  Google Scholar 

  • Thames, A. D., Kuhn, T. P., Mahmood, Z., Bilder, R. M., Williamson, T. J., Singer, E. J., & Arentoft, A. (2018). Effects of social adversity and HIV on subcortical shape and neurocognitive function. Brain Imaging and Behavior, 12(1), 96–108. https://doi.org/10.1007/s11682-017-9676-0.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson, P. M., Dutton, R. A., Hayaski, K. M., Toga, A. W., Lopez, O. L., Aizenstein, H. J., & Becker, J. T. (2005). Thinning of the cerebral cortex visualized in HIV/AIDS reflects CD4+ T-lymphocyte decline. PNAS, 102(43), 15647–15652.

    Article  CAS  Google Scholar 

  • Thompson, P. M., Dutton, R. A., Hayashi, K. M., Lu, A., Lee, S. E., Lee, J. Y., et al. (2006). 3D mapping of ventricular and corpus callosum abnormalities in HIV/AIDS. Neuroimage, 31(1), 12–23.

    Article  Google Scholar 

  • Thurnher, M. M., & Post, M. J. D. (2008). The uses of structural neuroimaging in the brain in HIV1-infected patients. In K. Goodkin, P. Shapshak, & A. Verma (Eds.), The Spectrum of neuro-AIDS disorder: Pathophysiology, diagnosis and treatment (pp. 247–272). Washington DC: ASMPress.

    Google Scholar 

  • Towgood, K. J., Pitkanen, M., Kulasegaram, R., Fradera, A., Kumar, A., Soni, S., et al. (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. https://doi.org/10.1016/j.cortex.2011.03.006.

    Article  PubMed  Google Scholar 

  • Underwood, J., Cole, J. H., Caan, M., De Francesco, D., Leech, R., van Zoest, R. A., et al. (2017). Gray and White Matter Abnormalities in Treated Human Immunodeficiency Virus Disease and Their Relationship to Cognitive Function. Clinical Infectious Diseases, 65(3), 422–432. https://doi.org/10.1093/cid/cix301.

    Article  PubMed  PubMed Central  Google Scholar 

  • Valcour, V., Busovaca, E., Wendeken, L., Esmareili, P., Rankin, K. P., Lobach, I., & Rosen, H. (2013). Brain white matter lesions link to CVD risk but not HIV factors in HIV over age 60. Journal of Neurovirology, 19, S1–S85.

    Google Scholar 

  • Wang, Y., Zhang, J., Gutman, B., Chan, T. F., Becker, J. T., Aizenstein, H. J., et al. (2009). Multivariate tensor-based morphometry on surfaces: Application to mapping ventricular abnormalities in HIV/AIDS. NeuroImage.

  • Wilson, T. W., Fox, H. S., Robertson, K. R., Sandkovsky, U., O'Neill, J., Heinrichs-Graham, E., et al. (2013). Abnormal MEG oscillatory activity during visual processing in the prefrontal cortices and frontal eye-fields of the aging HIV brain. PLoS One, 8(6), e66241. https://doi.org/10.1371/journal.pone.0066241.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson, T. W., Heinrichs-Graham, E., Becker, K. M., Aloi, J., Robertson, K. R., Sandkovsky, U., et al. (2015). Multimodal neuroimaging evidence of alterations in cortical structure and function in HIV-infected older adults. Human Brain Mapping, 36(3), 897–910. https://doi.org/10.1002/hbm.22674.

    Article  PubMed  Google Scholar 

  • Yiannoutsos, C. T., Ernst, T., Chang, L., Lee, P. L., Richards, T., Marra, C. M., et al. (2004). Regional patterns of brain metabolites in AIDS dementia complex. Neuroimage, 23(3), 928–935.

    Article  Google Scholar 

Download references

Acknowledgements

The preparation of this manuscript and the collection of the MRI data were supported in part by funds from the NIH to J.T.B. (AG034852 and MH098745).

Data in this manuscript were collected by the Multicenter AIDS Cohort Study (MACS) with centers at Baltimore (U01-AI35042): The Johns Hopkins University Bloomberg School of Public Health: Joseph B. Margolick (PI), Jay Bream, Todd Brown, Adrian Dobs, Michelle Estrella, W. David Hardy, Lisette Johnson-Hill, Sean Leng, Anne Monroe, Cynthia Munro, Michael W. Plankey, Wendy Post, Ned Sacktor, Jennifer Schrack, Chloe Thio; Chicago (U01-AI35039): Feinberg School of Medicine, Northwestern University, and Cook County Bureau of Health Services: Steven M. Wolinsky (PI), Sheila Badri, Dana Gabuzda, Frank J. Palella, Jr., Sudhir Penugonda, John P. Phair, Susheel Reddy, Matthew Stephens, Linda Teplin; Los Angeles (U01-AI35040): University of California, UCLA Schools of Public Health and Medicine: Roger Detels (PI), Otoniel Martínez-Maza (PI), Peter Anton, Robert Bolan, Elizabeth Breen, Anthony Butch, Shehnaz Hussain, Beth Jamieson, John Oishi, Harry Vinters, Dorothy Wiley, Mallory Witt, Otto Yang, Stephen Young, Zuo Feng Zhang; Pittsburgh (U01-AI35041): University of Pittsburgh, Graduate School of Public Health: Charles R. Rinaldo (PI), James T. Becker, Phalguni Gupta, Kenneth Ho, Lawrence A. Kingsley, Susan Koletar, Jeremy J. Martinson, John W. Mellors, Anthony J. Silvestre, Ronald D. Stall; Data Coordinating Center (UM1-AI35043): The Johns Hopkins University Bloomberg School of Public Health: Lisa P. Jacobson (PI), Gypsyamber D’Souza (PI), Alison Abraham, Keri Althoff, Michael Collaco, Priya Duggal, Sabina Haberlen, Eithne Keelaghan, Heather McKay, Alvaro Muñoz, Derek Ng, Anne Rostich, Eric C. Seaberg, Sol Su, Pamela Surkan, Nicholas Wada. Institute of Allergy and Infectious Diseases: Robin E. Huebner; National Cancer Institute: Geraldina Dominguez. The MACS is funded primarily by the National Institute of Allergy and Infectious Diseases (NIAID), with additional co-funding from the National Cancer Institute (NCI), the National Institute on Drug Abuse (NIDA), and the National Institute of Mental Health (NIMH). Targeted supplemental funding for specific projects was also provided by the National Heart, Lung, and Blood Institute (NHLBI), and the National Institute on Deafness and Communication Disorders (NIDCD). MACS data collection is also supported by UL1-TR001079 (JHU ICTR) from the National Center for Advancing Translational Sciences (NCATS) a component of the National Institutes of Health (NIH), and NIH Roadmap for Medical Research. The contents of this publication are solely the responsibility of the authors and do not represent the official views of the National Institutes of Health (NIH), Johns Hopkins ICTR, or NCATS. The MACS website is located at http://aidscohortstudy.org/.

The members of the Neuropsychology Working Group include Francine Barrington, James T. Becker, Pim Brouwers, Velpandi Ayyavoo, Karl Goodkin, Robin Huebner, Eithne Keelaghan, Andrew J. Levine, Eileen M. Martin, Cynthia Munro, Ann Ragin, Leah Rubin, Ned Sacktor, Eric Seaberg, and Carlie Williams.

Funding

AG034852, MH098745, U01-AI35042, U01-AI35039, U01-AI35040, UM1-AI35043, U01-AI35041

Author information

Author notes

  1. Mikhail Popov

    Present address: Wikimedia Foundation, San Francisco, CA, USA

Authors and Affiliations

  1. Department of Psychiatry, University of Pittsburgh, Suite 830, 3501 Forbes Avenue, Pittsburgh, PA, 15213, USA

    Mikhail Popov, Samantha A. Molsberry & James T. Becker

  2. Population Health Sciences, Harvard University, Cambridge, MA, USA

    Samantha A. Molsberry

  3. Department of Statistics, Carnegie Mellon University, Pittsburgh, PA, USA

    Fabrizio Lecci & Brian Junker

  4. Uber, New York, NY, USA

    Fabrizio Lecci

  5. Department of Infectious Diseases and Microbiology, University of Pittsburgh, Pittsburgh, PA, USA

    Lawrence A. Kingsley

  6. Department of Neurology, University of California Los Angeles, Los Angeles, CA, USA

    Andrew Levine

  7. Department of Psychiatry, Rush Medical School, Chicago, IL, USA

    Eileen Martin

  8. Department of Psychiatry, University of California Los Angeles, Los Angeles, CA, USA

    Eric Miller

  9. Department of Psychiatry, The Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Cynthia A. Munro

  10. Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Cynthia A. Munro & Ned Sacktor

  11. Department of Radiology, Northwestern University, Evanston, IL, USA

    Ann Ragin

  12. Department of Epidemiology, The Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA

    Eric Seaberg

  13. Department of Neurology, University of Pittsburgh, Pittsburgh, PA, USA

    James T. Becker

  14. Department of Psychology, University of Pittsburgh, Pittsburgh, PA, USA

    James T. Becker

Authors
  1. Mikhail Popov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samantha A. Molsberry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fabrizio Lecci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brian Junker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lawrence A. Kingsley
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andrew Levine
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eileen Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eric Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Cynthia A. Munro
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ann Ragin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Eric Seaberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ned Sacktor
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. James T. Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James T. Becker.

Ethics declarations

Conflict of interest

None

Ethical approval

This research was reviewed and approved by the Institutional Review Boards at all four MACS clinic sites – Johns Hopkins University, Northwestern University, University of California Los Angeles, and the University of Pittsburgh.

Informed consent

Each participant signed a written statement of informed consent prior to starting any research-related activities.

Disclosure

Eric N. Miller is the author of the reaction time software used in this study (CalCAP) and has a financial interest in the software.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOC 309 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Popov, M., Molsberry, S.A., Lecci, F. et al. Brain structural correlates of trajectories to cognitive impairment in men with and without HIV disease. Brain Imaging and Behavior 14, 821–829 (2020). https://doi.org/10.1007/s11682-018-0026-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-018-0026-7

Keywords

Search

Navigation