Skip to main content

Advertisement

SpringerLink
Log in

Neuroimaging and immunological features of neurocognitive function related to substance use in people with HIV

  • Published:
Journal of NeuroVirology Aims and scope Submit manuscript

Abstract

This study sought to identify neuroimaging and immunological factors associated with substance use and that contribute to neurocognitive impairment (NCI) in people with HIV (PWH). We performed cross-sectional immunological phenotyping, neuroimaging, and neurocognitive testing on virally suppressed PWH in four substance groups: cocaine only users (COC), marijuana only users (MJ), dual users (Dual), and Non-users. Participants completed substance use assessments, multimodal MRI brain scan, neuropsychological testing, and blood and CSF sampling. We employed a two-stage analysis of 305 possible biomarkers of cognitive function associated with substance use. Feature reduction (Kruskal Wallis p-value < 0.05) identified 53 biomarkers associated with substance use (22 MRI and 31 immunological) for model inclusion along with clinical and demographic variables. We employed eXtreme Gradient Boosting (XGBoost) with these markers to predict cognitive function (global T-score). SHapley Additive exPlanations (SHAP) values were calculated to rank features for impact on model output and NCI. Participants were 110 PWH with sustained HIV viral suppression (33 MJ, 12 COC, 22 Dual, and 43 Non-users). The ten highest ranking biomarkers for predicting global T-score were 4 neuroimaging biomarkers including functional connectivity, gray matter volume, and white matter integrity; 5 soluble biomarkers (plasma glycine, alanine, lyso-phosphatidylcholine (lysoPC) aC17.0, hydroxy-sphingomyelin (SM.OH) C14.1, and phosphatidylcholinediacyl (PC aa) C28.1); and 1 clinical variable (nadir CD4 count). The results of our machine learning model suggest that substance use may indirectly contribute to NCI in PWH through both metabolomic and neuropathological mechanisms.

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
Fig. 4

Similar content being viewed by others

References

  • Abdulle S, Mellgren A, Brew BJ, Cinque P, Hagberg L, Price RW, Rosengren L, Gisslen M (2007) CSF neurofilament protein (NFL) – a marker of active HIV-related neurodegeneration. J Neurol 254(8):1026–1032. https://doi.org/10.1007/s00415-006-0481-8

    Article  CAS  PubMed  Google Scholar 

  • Alakkas A, Ellis RJ, Watson CW, Umlauf A, Heaton RK, Letendre S, Collier A, Marra C, Clifford DB, Gelman B, Sacktor N, Morgello S, Simpson D, McCutchan JA, Kallianpur A, Gianella S, Marcotte T, Grant I, Fennema-Notestine C and Group C (2019) White matter damage, neuroinflammation, and neuronal integrity in HAND. J Neurovirol 25(1):32–41. https://doi.org/10.1007/s13365-018-0682-9

    Article  CAS  Google Scholar 

  • Anderson AM, Harezlak J, Bharti A, Mi D, Taylor MJ, Daar ES, Schifitto G, Zhong J, Alger JR, Brown MS, Singer EJ, Campbell TB, McMahon DD, Buchthal S, Cohen R, Yiannoutsos C, Letendre SL, Navia BA and Consortium HIVN (2015) Plasma and cerebrospinal fluid biomarkers predict cerebral injury in HIV-infected individuals on stable combination antiretroviral therapy. J Acquir Immune Defic Syndr 69(1):29–35. https://doi.org/10.1097/QAI.0000000000000532

    Article  CAS  Google Scholar 

  • Andersson JLR, Jenkinson M, Smith S (2007) Non-linear optimisation. FMRIB Technial Report TR07JA1. Oxford, United Kingdom, FMRIB Centre

  • 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(18):1789–1799. https://doi.org/10.1212/01.WNL.0000287431.88658.8b

    Article  CAS  PubMed  Google Scholar 

  • Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54(3):2033–2044. https://doi.org/10.1016/j.neuroimage.2010.09.025

    Article  PubMed  Google Scholar 

  • Bandaru VV, Mielke MM, Sacktor N, McArthur JC, Grant I, Letendre S, Chang L, Wojna V, Pardo C, Calabresi P, Munsaka S, Haughey NJ (2013) A lipid storage-like disorder contributes to cognitive decline in HIV-infected subjects. Neurology 81(17):1492–1499. https://doi.org/10.1212/WNL.0b013e3182a9565e

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benedict RHB (1997) Brief Visuospatial Memory Test-Revised Professional Manual. FL, Psychological Assessment Resources Inc, Odessa

    Google Scholar 

  • Benton A, Hamsher K, Sivan A (1983) Multilingual Aphasia Examination. Iowa City, IA, AJA Associates

  • Berger M, Murdoch DM, Staats JS, Chan C, Thomas JP, Garrigues GE, Browndyke JN, Cooter M, Quinones QJ, Mathew JP, Weinhold KJ and Team M-PS (2019) Flow cytometry characterization of cerebrospinal fluid monocytes in patients with postoperative cognitive dysfunction: a pilot study. Anesth Analg 129(5):e150–e154. https://doi.org/10.1213/ANE.0000000000004179

    Article  CAS  Google Scholar 

  • Bergland AK, Proitsi P, Kirsebom BE, Soennesyn H, Hye A, Larsen AI, Xu J, Legido-Quigley C, Rajendran L, Fladby T, Aarsland D (2020) Exploration of plasma lipids in mild cognitive impairment due to Alzheimer’s disease. J Alzheimers Dis 77(3):1117–1127. https://doi.org/10.3233/JAD-200441

    Article  CAS  PubMed  Google Scholar 

  • Bora A, Ubaida Mohien C, Chaerkady R, Chang L, Rt M, Sacktor N, Haughey N, McArthur JC, Cotter R, Nath A, Graham DR (2014) Identification of putative biomarkers for HIV-associated neurocognitive impairment in the CSF of HIV-infected patients under cART therapy determined by mass spectrometry. J Neurovirol 20(5):457–465. https://doi.org/10.1007/s13365-014-0263-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandt J, Benedict RHB (2001) Hopkins Verbal Learning Test – revised professional manual. FL, Psychological Assessment Resources Inc, Lutz

    Google Scholar 

  • Bridel C, van Wieringen WN, Zetterberg H, Tijms BM, Teunissen CE, the NFLG, Alvarez-Cermeno JC, Andreasson U, Axelsson M, Backstrom DC, Bartos A, Bjerke M, Blennow K, Boxer A, Brundin L, Burman J, Christensen T, Fialova L, Forsgren L, Frederiksen JL, Gisslen M, Gray E, Gunnarsson M, Hall S, Hansson O, Herbert MK, Jakobsson J, Jessen-Krut J, Janelidze S, Johannsson G, Jonsson M, Kappos L, Khademi M, Khalil M, Kuhle J, Landen M, Leinonen V, Logroscino G, Lu CH, Lycke J, Magdalinou NK, Malaspina A, Mattsson N, Meeter LH, Mehta SR, Modvig S, Olsson T, Paterson RW, Perez-Santiago J, Piehl F, Pijnenburg YAL, Pyykko OT, Ragnarsson O, Rojas JC, Romme Christensen J, Sandberg L, Scherling CS, Schott JM, Sellebjerg FT, Simone IL, Skillback T, Stilund M, Sundstrom P, Svenningsson A, Tortelli R, Tortorella C, Trentini A, Troiano M, Turner MR, van Swieten JC, Vagberg M, Verbeek MM, Villar LM, Visser PJ, Wallin A, Weiss A, Wikkelso C, Wild EJ (2019) Diagnostic value of cerebrospinal fluid neurofilament light protein in neurology: a systematic review and meta-analysis. JAMA Neurol 76(9):1035–1048. https://doi.org/10.1001/jamaneurol.2019.1534

  • Bryant AK, Moore DJ, Burdo TH, Lakritz JR, Gouaux B, Soontornniyomkij V, Achim CL, Masliah E, Grant I, Levine AJ, Ellis RJ (2017) Plasma soluble CD163 is associated with postmortem brain pathology in human immunodeficiency virus infection. AIDS 31(7):973–979. https://doi.org/10.1097/QAD.0000000000001425

    Article  CAS  PubMed  Google Scholar 

  • Burdo TH, Weiffenbach A, Woods SP, Letendre S, Ellis RJ, Williams KC (2013) Elevated sCD163 in plasma but not cerebrospinal fluid is a marker of neurocognitive impairment in HIV infection. AIDS 27(9):1387–1395. https://doi.org/10.1097/QAD.0b013e32836010bd

    Article  CAS  PubMed  Google Scholar 

  • Byrd DA, Fellows RP, Morgello S, Franklin D, Heaton RK, Deutsch R, Atkinson JH, Clifford DB, Collier AC, Marra CM, Gelman B, McCutchan JA, Duarte NA, Simpson DM, McArthur J, Grant I and Group C (2011) Neurocognitive impact of substance use in HIV infection. J Acquir Immune Defic Syndr 58(2):154–162. https://doi.org/10.1097/QAI.0b013e318229ba41

    Article  Google Scholar 

  • Chen T, Guestrin C (2016) XGBoost: a scalable tree boosting system. Proceedings of the 22nd ACM SIGKDD International Conference on Knowledge Discovery and Data Mining. San Francisco, California, USA, Association for Computing Machinery: 785–794

  • Cheng H, Skosnik PD, Pruce BJ, Brumbaugh MS, Vollmer JM, Fridberg DJ, O’Donnell BF, Hetrick WP, Newman SD (2014) Resting state functional magnetic resonance imaging reveals distinct brain activity in heavy cannabis users - a multi-voxel pattern analysis. J Psychopharmacol 28(11):1030–1040. https://doi.org/10.1177/0269881114550354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cristiani SA, Pukay-Martin ND, Bornstein RA (2004) Marijuana use and cognitive function in HIV-infected people. J Neuropsychiatry Clin Neurosci 16(3):330–335. https://doi.org/10.1176/jnp.16.3.330

    Article  PubMed  Google Scholar 

  • Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9(2):179–194. https://doi.org/10.1006/nimg.1998.0395

    Article  CAS  PubMed  Google Scholar 

  • Dale AM, Sereno MI (1993) Improved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 5(2):162–176. https://doi.org/10.1162/jocn.1993.5.2.162

    Article  CAS  PubMed  Google Scholar 

  • Davies O, Haynes BI, Casey SJ, Gerbase S, Barker GJ, Pitkanen M, Kulasegaram R, Kopelman MD (2019) Clinical and neuroimaging correlates of cognition in HIV. J Neurovirol 25(6):754–764. https://doi.org/10.1007/s13365-019-00763-w

    Article  PubMed  PubMed Central  Google Scholar 

  • Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31(3):968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021

    Article  PubMed  Google Scholar 

  • Diaz PT, Wewers MD, King M, Wade J, Hart J, Clanton TL (2004) Regional differences in emphysema scores and BAL glutathione levels in HIV-infected individuals. Chest 126(5):1439–1442. https://doi.org/10.1378/chest.126.5.1439

    Article  PubMed  Google Scholar 

  • Diehl P, Nienaber F, Zaldivia MTK, Stamm J, Siegel PM, Mellett NA, Wessinger M, Wang X, McFadyen JD, Bassler N, Puetz G, Htun NM, Braig D, Habersberger J, Helbing T, Eisenhardt SU, Fuller M, Bode C, Meikle PJ, Chen YC, Peter K (2019) Lysophosphatidylcholine is a major component of platelet microvesicles promoting platelet activation and reporting atherosclerotic plaque instability. Thromb Haemost 119(8):1295–1310. https://doi.org/10.1055/s-0039-1683409

    Article  PubMed  Google Scholar 

  • Diehr MC, Cherner M, Wolfson TJ, Miller SW, Grant I, Heaton RK and Group HIVNRC (2003) The 50 and 100-item short forms of the Paced Auditory Serial Addition Task (PASAT): demographically corrected norms and comparisons with the full PASAT in normal and clinical samples. J Clin Exp Neuropsychol 25(4):571–585. https://doi.org/10.1076/jcen.25.4.571.13876

    Article  Google Scholar 

  • Ellis RJ, Badiee J, Vaida F, Letendre S, Heaton RK, Clifford D, Collier AC, Gelman B, McArthur J, Morgello S, McCutchan JA, Grant I and Group C (2011) CD4 nadir is a predictor of HIV neurocognitive impairment in the era of combination antiretroviral therapy. AIDS 25(14):1747–1751. https://doi.org/10.1097/QAD.0b013e32834a40cd

    Article  CAS  Google Scholar 

  • Ellis RJ, Peterson S, Cherner M, Morgan E, Schrier R, Tang B, Hoenigl M, Letendre S, Iudicello J (2021) Beneficial effects of cannabis on blood-brain barrier function in human immunodeficiency virus. Clin Infect Dis 73(1):124–129. https://doi.org/10.1093/cid/ciaa437

    Article  CAS  PubMed  Google Scholar 

  • Ellis RJ, Peterson SN, Li Y, Schrier R, Iudicello J, Letendre S, Morgan E, Tang B, Grant I, Cherner M (2020) Recent cannabis use in HIV is associated with reduced inflammatory markers in CSF and blood. Neurol Neuroimmunol Neuroinflamm 7(5). https://doi.org/10.1212/NXI.0000000000000809.

  • Ersche KD, Barnes A, Jones PS, Morein-Zamir S, Robbins TW, Bullmore ET (2011) Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence. Brain 134(Pt 7):2013–2024. https://doi.org/10.1093/brain/awr138

    Article  PubMed  PubMed Central  Google Scholar 

  • Feltenstein MW, See RE (2008) The neurocircuitry of addiction: an overview. Br J Pharmacol 154(2):261–274. https://doi.org/10.1038/bjp.2008.51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filbey FM, Aslan S, Calhoun VD, Spence JS, Damaraju E, Caprihan A, Segall J (2014) Long-term effects of marijuana use on the brain. Proc Natl Acad Sci U S A 111(47):16913–16918. https://doi.org/10.1073/pnas.1415297111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • First MB, Williams JBW, Karg RS, Spitzer RL (2015) Structured Clinical Interview for DSM-5—Research Version (SCID-5 for DSM-5, Research Version; SCID-5-RV). Arlington, VA, American Psychiatric Association

  • Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 97(20):11050–11055. https://doi.org/10.1073/pnas.200033797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20(1):70–80. https://doi.org/10.1109/42.906426

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355. https://doi.org/10.1016/s0896-6273(02)00569-x

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, Salat DH, van der Kouwe AJ, Makris N, Segonne F, Quinn BT, Dale AM (2004a) Sequence-independent segmentation of magnetic resonance images. Neuroimage 23(Suppl 1):S69-84. https://doi.org/10.1016/j.neuroimage.2004.07.016

    Article  PubMed  Google Scholar 

  • Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004b) Automatically parcellating the human cerebral cortex. Cereb Cortex 14(1):11–22. https://doi.org/10.1093/cercor/bhg087

    Article  PubMed  Google Scholar 

  • Fote G, Wu J, Mapstone M, Macciardi F, Fiandaca MS, Federoff HJ (2021) Plasma sphingomyelins in late-onset Alzheimer’s disease. J Alzheimers Dis 83(3):1161–1171. https://doi.org/10.3233/JAD-200871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Y, Wang H, Huff TB, Shi R, Cheng JX (2007) Coherent anti-Stokes Raman scattering imaging of myelin degradation reveals a calcium-dependent pathway in lyso-PtdCho-induced demyelination. J Neurosci Res 85(13):2870–2881. https://doi.org/10.1002/jnr.21403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garza-Villarreal EA, Chakravarty MM, Hansen B, Eskildsen SF, Devenyi GA, Castillo-Padilla D, Balducci T, Reyes-Zamorano E, Jespersen SN, Perez-Palacios P, Patel R, Gonzalez-Olvera JJ (2017) The effect of crack cocaine addiction and age on the microstructure and morphology of the human striatum and thalamus using shape analysis and fast diffusion kurtosis imaging. Transl Psychiatry 7(5):e1122. https://doi.org/10.1038/tp.2017.92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gisslen M, Price RW, Andreasson U, Norgren N, Nilsson S, Hagberg L, Fuchs D, Spudich S, Blennow K, Zetterberg H (2016) Plasma concentration of the neurofilament light protein (NFL) is a biomarker of CNS injury in HIV infection: a cross-sectional study. EBioMedicine 3:135–140. https://doi.org/10.1016/j.ebiom.2015.11.036

    Article  PubMed  Google Scholar 

  • Golden CJ (1978) Stroop Color and Word Test. IL, Stoelting, Chicago

    Google Scholar 

  • Grauer OM, Reichelt D, Gruneberg U, Lohmann H, Schneider-Hohendorf T, Schulte-Mecklenbeck A, Gross CC, Meuth SG, Wiendl H, Husstedt IW (2015) Neurocognitive decline in HIV patients is associated with ongoing T-cell activation in the cerebrospinal fluid. Ann Clin Transl Neurol 2(9):906–919. https://doi.org/10.1002/acn3.227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall SA, Lalee Z, Bell RP, Towe SL, Meade CS (2021) Synergistic effects of HIV and marijuana use on functional brain network organization. Prog Neuropsychopharmacol Biol Psychiatry 104:110040. https://doi.org/10.1016/j.pnpbp.2020.110040

    Article  PubMed  Google Scholar 

  • Han X, Rozen S, Boyle SH, Hellegers C, Cheng H, Burke JR, Welsh-Bohmer KA, Doraiswamy PM, Kaddurah-Daouk R (2011) Metabolomics in early Alzheimer’s disease: identification of altered plasma sphingolipidome using shotgun lipidomics. PLoS ONE 6(7):e21643. https://doi.org/10.1371/journal.pone.0021643

    Article  CAS  PubMed  PubMed Central  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 and Group C (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 75(23):2087–2096. https://doi.org/10.1212/WNL.0b013e318200d727

    Article  PubMed  PubMed Central  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, Group C and Group H (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 17(1):3–16. https://doi.org/10.1007/s13365-010-0006-1

  • Heaton RK, Franklin DR, Jr., Deutsch R, Letendre S, Ellis RJ, Casaletto K, Marquine MJ, Woods SP, Vaida F, Atkinson JH, Marcotte TD, McCutchan JA, Collier AC, Marra CM, Clifford DB, Gelman BB, Sacktor N, Morgello S, Simpson DM, Abramson I, Gamst AC, Fennema-Notestine C, Smith DM, Grant I and Group C (2015) Neurocognitive change in the era of HIV combination antiretroviral therapy: the longitudinal CHARTER study. Clin Infect Dis 60(3):473–480. https://doi.org/10.1093/cid/ciu862

    Article  CAS  Google Scholar 

  • Heaton RK, Miller SW, Taylor MJ, Grant I (2004) Revised comprehensive norms for an expanded Halstead-Reitan battery: demographically adjusted neuropsychological norms for African American and Caucasian adults. FL, Psychological Assessment Resources Inc, Lutz

    Google Scholar 

  • Hileman CO, Kalayjian RC, Azzam S, Schlatzer D, Wu K, Tassiopoulos K, Bedimo R, Ellis RJ, Erlandson KM, Kallianpur A, Koletar SL, Landay AL, Palella FJ, Taiwo B, Pallaki M, Hoppel CL (2021) Plasma citrate and succinate are associated with neurocognitive impairment in older people with HIV. Clin Infect Dis 73(3):e765–e772. https://doi.org/10.1093/cid/ciab107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ipser JC, Brown GG, Bischoff-Grethe A, Connolly CG, Ellis RJ, Heaton RK, Grant I, Translational Methamphetamine ARCG (2015) HIV infection is associated with attenuated frontostriatal intrinsic connectivity: a preliminary study. J Int Neuropsychol Soc 21(3):203–213. https://doi.org/10.1017/S1355617715000156

    Article  PubMed  PubMed Central  Google Scholar 

  • Israel SM, Hassanzadeh-Behbahani S, Turkeltaub PE, Moore DJ, Ellis RJ, Jiang X (2019) Different roles of frontal versus striatal atrophy in HIV-associated neurocognitive disorders. Hum Brain Mapp 40(10):3010–3026. https://doi.org/10.1002/hbm.24577

    Article  PubMed  PubMed Central  Google Scholar 

  • Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62(2):782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015

    Article  PubMed  Google Scholar 

  • Jessen Krut J, Mellberg T, Price RW, Hagberg L, Fuchs D, Rosengren L, Nilsson S, Zetterberg H, Gisslen M (2014) Biomarker evidence of axonal injury in neuroasymptomatic HIV-1 patients. PLoS ONE 9(2):e88591. https://doi.org/10.1371/journal.pone.0088591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JD, Kuhn T, Mahmood Z, Singer EJ, Hinkin CH, Thames AD (2018) Longitudinal intra-individual variability in neuropsychological performance relates to white matter changes in HIV. Neuropsychology 32(2):206–212. https://doi.org/10.1037/neu0000390

    Article  PubMed  Google Scholar 

  • Kallianpur KJ, Jahanshad N, Sailasuta N, Benjapornpong K, Chan P, Pothisri M, Dumrongpisutikul N, Laws E, Ndhlovu LC, Clifford KM, Paul R, Jagodzinski L, Krebs S, Ananworanich J, Spudich S, Valcour V and Group SRS (2020) Regional brain volumetric changes despite 2 years of treatment initiated during acute HIV infection. AIDS 34(3):415–426. https://doi.org/10.1097/QAD.0000000000002436

    Article  CAS  Google Scholar 

  • Kato T, Yoshihara Y, Watanabe D, Fukumoto M, Wada K, Nakakura T, Kuriyama K, Shirasaka T, Murai T (2020) Neurocognitive impairment and gray matter volume reduction in HIV-infected patients. J Neurovirol 26(4):590–601. https://doi.org/10.1007/s13365-020-00865-w

    Article  CAS  PubMed  Google Scholar 

  • Klove H (1963) Gooved Pegboard. Lafayette, IN, Lafayette Instruments

  • Knuplez E, Marsche G (2020) An updated review of pro- and anti-inflammatory properties of plasma lysophosphatidylcholines in the vascular system. Int J Mol Sci 21(12). https://doi.org/10.3390/ijms21124501.

  • Kongs SK, Thompson LL, Iverson GL, Heaton RK (2000) Wisconsin Card Sorting Test-64 Computerized Version. FL, Psychological Assessment Resources Inc, Odessa

    Google Scholar 

  • Lundberg SM, Erion G, Chen H, DeGrave A, Prutkin JM, Nair B, Katz R, Himmelfarb J, Bansal N, Lee S-I (2020) From local explanations to global understanding with explainable AI for trees. Nature Machine Intelligence 2(1):56–67. https://doi.org/10.1038/s42256-019-0138-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Lundberg SM, Lee S (2017) A unified approach to interpreting model predictions. 31st Conference on Neural Information Processing Systems (NIPS 2017). Long Beach, CA, USA

  • Lyons JL, Uno H, Ancuta P, Kamat A, Moore DJ, Singer EJ, Morgello S, Gabuzda D (2011) Plasma sCD14 is a biomarker associated with impaired neurocognitive test performance in attention and learning domains in HIV infection. J Acquir Immune Defic Syndr 57(5):371–379. https://doi.org/10.1097/QAI.0b013e3182237e54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mackey S, Allgaier N, Chaarani B, Spechler P, Orr C, Bunn J, Allen NB, Alia-Klein N, Batalla A, Blaine S, Brooks S, Caparelli E, Chye YY, Cousijn J, Dagher A, Desrivieres S, Feldstein-Ewing S, Foxe JJ, Goldstein RZ, Goudriaan AE, Heitzeg MM, Hester R, Hutchison K, Korucuoglu O, Li CR, London E, Lorenzetti V, Luijten M, Martin-Santos R, May A, Momenan R, Morales A, Paulus MP, Pearlson G, Rousseau ME, Salmeron BJ, Schluter R, Schmaal L, Schumann G, Sjoerds Z, Stein DJ, Stein EA, Sinha R, Solowij N, Tapert S, Uhlmann A, Veltman D, van Holst R, Whittle S, Wright MJ, Yucel M, Zhang S, Yurgelun-Todd D, Hibar DP, Jahanshad N, Evans A, Thompson PM, Glahn DC, Conrod P, Garavan H and Group EAW (2019) Mega-analysis of gray matter volume in substance dependence: general and substance-specific regional effects. Am J Psychiatry 176(2):119–128. https://doi.org/10.1176/appi.ajp.2018.17040415

  • Manza P, Tomasi D, Volkow ND (2018) Subcortical local functional hyperconnectivity in cannabis dependence. Biol Psychiatry Cogn Neurosci Neuroimaging 3(3):285–293. https://doi.org/10.1016/j.bpsc.2017.11.004

    Article  PubMed  Google Scholar 

  • McLellan AT, Kushner H, Metzger D, Peters R, Smith I, Grissom G, Pettinati H, Argeriou M (1992) The Fifth Edition of the Addiction Severity Index. J Subst Abuse Treat 9(3):199–213. https://doi.org/10.1016/0740-5472(92)90062-s

  • Meade CS, Towe SL, Skalski LM, Robertson KR (2015) Independent effects of HIV infection and cocaine dependence on neurocognitive impairment in a community sample living in the southern United States. Drug Alcohol Depend 149:128–135. https://doi.org/10.1016/j.drugalcdep.2015.01.034

    Article  PubMed  PubMed Central  Google Scholar 

  • Mehta SR, Perez-Santiago J, Hulgan T, Day TR, Barnholtz-Sloan J, Gittleman H, Letendre S, Ellis R, Heaton R, Patton S, Suben JD, Franklin D, Rosario D, Clifford DB, Collier AC, Marra CM, Gelman BB, McArthur J, McCutchan A, Morgello S, Simpson D, Connor J, Grant I, Kallianpur A (2017) Cerebrospinal fluid cell-free mitochondrial DNA is associated with HIV replication, iron transport, and mild HIV-associated neurocognitive impairment. J Neuroinflammation 14(1):72. https://doi.org/10.1186/s12974-017-0848-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mimiaga MJ, Reisner SL, Grasso C, Crane HM, Safren SA, Kitahata MM, Schumacher JE, Mathews WC, Mayer KH (2013) Substance use among HIV-infected patients engaged in primary care in the United States: findings from the Centers for AIDS Research Network of Integrated Clinical Systems cohort. Am J Public Health 103(8):1457–1467. https://doi.org/10.2105/AJPH.2012.301162

    Article  PubMed  PubMed Central  Google Scholar 

  • Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga AW, Pike GB, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl P, Mazziotta J (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40(2):570–582. https://doi.org/10.1016/j.neuroimage.2007.12.035

    Article  PubMed  Google Scholar 

  • Nestler EJ (2005) Is there a common molecular pathway for addiction? Nat Neurosci 8(11):1445–1449. https://doi.org/10.1038/nn1578

    Article  CAS  PubMed  Google Scholar 

  • Newman LM, Trivedi MA, Bendlin BB, Ries ML, Johnson SC (2007) The relationship between gray matter morphometry and neuropsychological performance in a large sample of cognitively healthy adults. Brain Imaging Behav 1(1–2):3–10. https://doi.org/10.1007/s11682-007-9000-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Nickerson LD, Smith SM, Ongur D, Beckmann CF (2017) Using dual regression to investigate network shape and amplitude in functional connectivity analyses. Front Neurosci 11:115. https://doi.org/10.3389/fnins.2017.00115

    Article  PubMed  PubMed Central  Google Scholar 

  • Nir TM, Jahanshad N, Ching CRK, Cohen RA, Harezlak J, Schifitto G, Lam HY, Hua X, Zhong J, Zhu T, Taylor MJ, Campbell TB, Daar ES, Singer EJ, Alger JR, Thompson PM, Navia BA, Consortium HIVN (2019) Progressive brain atrophy in chronically infected and treated HIV+ individuals. J Neurovirol 25(3):342–353. https://doi.org/10.1007/s13365-019-00723-4

  • Nobuhara CK, Bullock WM, Bunning T, Colin B, Cooter M, Devinney MJ, Ferrandino MN, Gadsden J, Garrigues G, Habib AS, Moretti E, Moul J, Ohlendorf B, Sandler A, Scheri R, Sharma B, Thomas JP, Young C, Mathew JP, Berger M, Madco PC and Teams II (2020) A protocol to reduce self-reported pain scores and adverse events following lumbar punctures in older adults. J Neurol 267(7):2002–2006. https://doi.org/10.1007/s00415-020-09797-1

  • O’Connor EE, Zeffiro TA, Zeffiro TA (2018) Brain structural changes following HIV infection: meta-analysis. AJNR Am J Neuroradiol 39(1):54–62. https://doi.org/10.3174/ajnr.A5432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogonor E, Abiodun P, Sadoh W (2021) Evaluation of glutathione levels in HIV infected children in Benin City, Nigeria. West Afr J Med 38(8):719–725

    CAS  PubMed  Google Scholar 

  • Oguz I, Farzinfar M, Matsui J, Budin F, Liu Z, Gerig G, Johnson HJ, Styner M (2014) DTIPrep: quality control of diffusion-weighted images. Front Neuroinform 8:4. https://doi.org/10.3389/fninf.2014.00004

    Article  PubMed  PubMed Central  Google Scholar 

  • Osuch EA, Manning K, Hegele RA, Theberge J, Neufeld R, Mitchell D, Williamson P, Gardner RC (2016) Depression, marijuana use and early-onset marijuana use conferred unique effects on neural connectivity and cognition. Acta Psychiatr Scand 134(5):399–409. https://doi.org/10.1111/acps.12629

    Article  CAS  PubMed  Google Scholar 

  • Peluso MJ, Meyerhoff DJ, Price RW, Peterson J, Lee E, Young AC, Walter R, Fuchs D, Brew BJ, Cinque P, Robertson K, Hagberg L, Zetterberg H, Gisslen M, Spudich S (2013) Cerebrospinal fluid and neuroimaging biomarker abnormalities suggest early neurological injury in a subset of individuals during primary HIV infection. J Infect Dis 207(11):1703–1712. https://doi.org/10.1093/infdis/jit088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Santiago J, Schrier RD, de Oliveira MF, Gianella S, Var SR, Day TR, Ramirez-Gaona M, Suben JD, Murrell B, Massanella M, Cherner M, Smith DM, Ellis RJ, Letendre SL, Mehta SR (2016) Cell-free mitochondrial DNA in CSF is associated with early viral rebound, inflammation, and severity of neurocognitive deficits in HIV infection. J Neurovirol 22(2):191–200. https://doi.org/10.1007/s13365-015-0384-5

    Article  CAS  PubMed  Google Scholar 

  • Plemel JR, Michaels NJ, Weishaupt N, Caprariello AV, Keough MB, Rogers JA, Yukseloglu A, Lim J, Patel VV, Rawji KS, Jensen SK, Teo W, Heyne B, Whitehead SN, Stys PK, Yong VW (2018) Mechanisms of lysophosphatidylcholine-induced demyelination: a primary lipid disrupting myelinopathy. Glia 66(2):327–347. https://doi.org/10.1002/glia.23245

    Article  PubMed  Google Scholar 

  • Pruim RHR, Mennes M, van Rooij D, Llera A, Buitelaar JK, Beckmann CF (2015) ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage 112:267–277. https://doi.org/10.1016/j.neuroimage.2015.02.064

    Article  PubMed  Google Scholar 

  • Python Software Foundation (2022)  The Python Language Reference — Python 3.11.0 documentation

  • R Core Team (2021) R: A Language and enironment for statistical computing. Austria, R Foundation for Stastical Computing, Vienna

    Google Scholar 

  • Ragin AB, Wu Y, Gao Y, Keating S, Du H, Sammet C, Kettering CS, Epstein LG (2015) Brain alterations within the first 100 days of HIV infection. Ann Clin Transl Neurol 2(1):12–21. https://doi.org/10.1002/acn3.136

    Article  PubMed  Google Scholar 

  • Reitan RM, Wolfson D (1993) The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. AZ, Neuropsychology Press, Tucson

    Google Scholar 

  • Reuter M, Rosas HD, Fischl B (2010) Highly accurate inverse consistent registration: a robust approach. Neuroimage 53(4):1181–1196. https://doi.org/10.1016/j.neuroimage.2010.07.020

    Article  PubMed  Google Scholar 

  • Rippeth JD, Heaton RK, Carey CL, Marcotte TD, Moore DJ, Gonzalez R, Wolfson T, Grant I and Group H (2004) Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. J Int Neuropsychol Soc 10(1):1–14. https://doi.org/10.1017/S1355617704101021

    Article  CAS  Google Scholar 

  • Ritchay MM, Huggins AA, Wallace AL, Larson CL, Lisdahl KM (2021) Resting state functional connectivity in the default mode network: Relationships between cannabis use, gender, and cognition in adolescents and young adults. Neuroimage Clin 30:102664. https://doi.org/10.1016/j.nicl.2021.102664

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson SM, Sobell LC, Sobell MB, Leo GI (2014) Reliability of the timeline followback for cocaine, cannabis, and cigarette use. Psychol Addict Behav 28(1):154–162. https://doi.org/10.1037/a0030992

    Article  PubMed  Google Scholar 

  • Samboju V, Philippi CL, Chan P, Cobigo Y, Fletcher JLK, Robb M, Hellmuth J, Benjapornpong K, Dumrongpisutikul N, Pothisri M, Paul R, Ananworanich J, Spudich S, Valcour V, Search RV, teams RVp (2018) Structural and functional brain imaging in acute HIV. Neuroimage Clin 20:327–335. https://doi.org/10.1016/j.nicl.2018.07.024

    Article  PubMed  PubMed Central  Google Scholar 

  • Schemmer P, Zhong Z, Galli U, Wheeler MD, Xiangli L, Bradford BU, Conzelmann LO, Forman D, Boyer J, Thurman RG (2013) Glycine reduces platelet aggregation. Amino Acids 44(3):925–931. https://doi.org/10.1007/s00726-012-1422-8

    Article  CAS  PubMed  Google Scholar 

  • Schrier RD, Hong S, Crescini M, Ellis R, Perez-Santiago J, Spina C, Letendre S and Group H (2015) Cerebrospinal fluid (CSF) CD8+ T-cells that express interferon-gamma contribute to HIV associated neurocognitive disorders (HAND). PLoS ONE 10(2):e0116526. https://doi.org/10.1371/journal.pone.0116526

    Article  CAS  Google Scholar 

  • Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004) A hybrid approach to the skull stripping problem in MRI. Neuroimage 22(3):1060–1075. https://doi.org/10.1016/j.neuroimage.2004.03.032

    Article  CAS  PubMed  Google Scholar 

  • Segonne F, Pacheco J, Fischl B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26(4):518–529. https://doi.org/10.1109/TMI.2006.887364

    Article  PubMed  Google Scholar 

  • Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD (2012) Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22(1):158–165. https://doi.org/10.1093/cercor/bhr099

    Article  CAS  PubMed  Google Scholar 

  • Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17(1):87–97. https://doi.org/10.1109/42.668698

    Article  CAS  PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31(4):1487–1505. https://doi.org/10.1016/j.neuroimage.2006.02.024

    Article  PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208-219. https://doi.org/10.1016/j.neuroimage.2004.07.051

    Article  PubMed  Google Scholar 

  • Sobell LC, Sobell MB (1996) Timeline follow-back user’s guide: a calendar method for assessing alcohol and drug use. Addiction Research Foundation, Toronto

    Google Scholar 

  • Stachlewitz RF, Li X, Smith S, Bunzendahl H, Graves LM, Thurman RG (2000) Glycine inhibits growth of T lymphocytes by an IL-2-independent mechanism. J Immunol 164(1):176–182. https://doi.org/10.4049/jimmunol.164.1.176

    Article  CAS  PubMed  Google Scholar 

  • Su T, Caan MW, Wit FW, Schouten J, Geurtsen GJ, Cole JH, Sharp DJ, Vos FM, Prins M, Portegies P, Reiss P, Majoie CB and Study AGC (2016) White matter structure alterations in HIV-1-infected men with sustained suppression of viraemia on treatment. AIDS 30(2):311–322. https://doi.org/10.1097/QAD.0000000000000945

    Article  CAS  Google Scholar 

  • Thomas JB, Brier MR, Snyder AZ, Vaida FF, Ances BM (2013) Pathways to neurodegeneration: effects of HIV and aging on resting-state functional connectivity. Neurology 80(13):1186–1193. https://doi.org/10.1212/WNL.0b013e318288792b

    Article  PubMed  PubMed Central  Google Scholar 

  • Tuck MK, Chan DW, Chia D, Godwin AK, Grizzle WE, Krueger KE, Rom W, Sanda M, Sorbara L, Stass S, Wang W, Brenner DE (2009) Standard operating procedures for serum and plasma collection: early detection research network consensus statement standard operating procedure integration working group. J Proteome Res 8(1):113–117. https://doi.org/10.1021/pr800545q

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ullah R, Jo MH, Riaz M, Alam SI, Saeed K, Ali W, Rehman IU, Ikram M, Kim MO (2020) Glycine, the smallest amino acid, confers neuroprotection against D-galactose-induced neurodegeneration and memory impairment by regulating c-Jun N-terminal kinase in the mouse brain. J Neuroinflammation 17(1):303. https://doi.org/10.1186/s12974-020-01989-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Underwood J, Cole JH, Caan M, De Francesco D, Leech R, van Zoest RA, Su T, Geurtsen GJ, Schmand BA, Portegies P, Prins M, Wit F, Sabin CA, Majoie C, Reiss P, Winston A, Sharp DJ, Comorbidity in Relation to AC (2017) Gray and white matter abnormalities in treated human immunodeficiency virus disease and their relationship to cognitive function. Clin Infect Dis 65(3):422–432. https://doi.org/10.1093/cid/cix301

    Article  PubMed  PubMed Central  Google Scholar 

  • Vassimon HS, Deminice R, Machado AA, Monteiro JP, Jordao AA (2010) The association of lipodystrophy and oxidative stress biomarkers in HIV-infected men. Curr HIV Res 8(5):364–369. https://doi.org/10.2174/157016210791330347

    Article  CAS  PubMed  Google Scholar 

  • Volkow ND, Fowler JS, Wang GJ, Swanson JM (2004) Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Mol Psychiatry 9(6):557–569. https://doi.org/10.1038/sj.mp.4001507

    Article  CAS  PubMed  Google Scholar 

  • Wechsler D (2008) Wechsler Adult Intelligence Scale. San Antonio, TX, Pearson Assessment

  • Wheeler MD, Rose ML, Yamashima S, Enomoto N, Seabra V, Madren J, Thurman RG (2000) Dietary glycine blunts lung inflammatory cell influx following acute endotoxin. Am J Physiol Lung Cell Mol Physiol 279(2):L390-398. https://doi.org/10.1152/ajplung.2000.279.2.L390

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Bai L, Zhou Y, Kang S, Liang P, Wang L, Zhu Y (2017) Increased inter-hemispheric resting-state functional connectivity in acute lacunar stroke patients with aphasia. Exp Brain Res 235(3):941–948. https://doi.org/10.1007/s00221-016-4851-x

    Article  CAS  PubMed  Google Scholar 

  • Yao H, Duan M, Buch S (2011a) Cocaine-mediated induction of platelet-derived growth factor: implication for increased vascular permeability. Blood 117(8):2538–2547. https://doi.org/10.1182/blood-2010-10-313593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao H, Kim K, Duan M, Hayashi T, Guo M, Morgello S, Prat A, Wang J, Su TP, Buch S (2011b) Cocaine hijacks sigma1 receptor to initiate induction of activated leukocyte cell adhesion molecule: implication for increased monocyte adhesion and migration in the CNS. J Neurosci 31(16):5942–5955. https://doi.org/10.1523/JNEUROSCI.5618-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan P, Raz N (2014) Prefrontal cortex and executive functions in healthy adults: a meta-analysis of structural neuroimaging studies. Neurosci Biobehav Rev 42:180–192. https://doi.org/10.1016/j.neubiorev.2014.02.005

    Article  PubMed  Google Scholar 

  • Zimmerman ME, Brickman AM, Paul RH, Grieve SM, Tate DF, Gunstad J, Cohen RA, Aloia MS, Williams LM, Clark CR, Whitford TJ, Gordon E (2006) The relationship between frontal gray matter volume and cognition varies across the healthy adult lifespan. Am J Geriatr Psychiatry 14(10):823–833. https://doi.org/10.1097/01.JGP.0000238502.40963.ac

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the study participants whose dedication made this research possible. We thank Cynthia Gay, Coleen Cunningham, Maren Olsen, Diane Bresch, and Jonathan Klus for their contextual and scientific input and study management. We would also like to thank the UNC and Duke Infectious Disease clinics and their study staff that made this work possible.

Funding

We wish to acknowledge support from the Biostatistics, Epidemiology and Research Design (BERD) Methods Core funded through Grant Award Number UL1TR002553 from the National Center for Advancing Translational Sciences (NCATS), a component of the NIH. This research was supported by the National Institutes for Health (NIH) grant R01DA043241.

Author information

Authors and Affiliations

  1. Department of Medicine, Duke University Medical Center, DUMC Box 2629, Durham, NC, 27710, USA

    David M. Murdoch, Alicia Volkheimer & Joyce Choe

  2. Department of Biostatistics and Bioinformatics, Duke University Medical Center, Durham, NC, USA

    Richard Barfield, Cliburn Chan & Jichun Xie

  3. Center for Human Systems Immunology, School of Medicine, Duke University, Durham, NC, USA

    Richard Barfield, Cliburn Chan & Jichun Xie

  4. Department of Psychiatry & Behavioral Sciences, Duke University Medical Center, Durham, NC, USA

    Sheri L. Towe, Ryan P. Bell, Shana A. Hall & Christina S. Meade

  5. Department of Anesthesiology, Duke University Medical Center, Durham, NC, USA

    Miles Berger

  6. Department of Mathematics, Duke University, Durham, NC, USA

    Jichun Xie

Authors
  1. David M. Murdoch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard Barfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cliburn Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sheri L. Towe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ryan P. Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alicia Volkheimer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joyce Choe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shana A. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Miles Berger
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jichun Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Christina S. Meade
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to manuscript preparation. Conceptualization: DM, CC, ST, MB, CM. Experimentation: DM, AV, JC. Patient recruitment: DM, ST, MB, CM. Data analysis: DM, RB, CC, ST, RB, SH, JX, CM. Supervision: DM, CC, CM. Manuscript writing: DM, RB, ST, CM.

Corresponding author

Correspondence to David M. Murdoch.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1432 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Murdoch, D.M., Barfield, R., Chan, C. et al. Neuroimaging and immunological features of neurocognitive function related to substance use in people with HIV. J. Neurovirol. 29, 78–93 (2023). https://doi.org/10.1007/s13365-022-01102-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13365-022-01102-2

Keywords

Search

Navigation