Human immunodeficiency virus infection in the CNS and decreased dopamine availability: relationship with neuropsychological performance

American Academy of Neurology (AAN) AIDS Task Force Working Group (1991) Nomenclature and research definition for neurological manifestations of human immunodeficiency virus type-1 (HIV-1) infection. Neurology 41:778–785

Ances BM, Ellis RJ (2007) Dementia and neurocognitive disorders due to HIV-1 infection. Seminar Neurol 27(1):86–92

Ances BM, Roc AC, Wang J, Korczykowski M, Okawa J, Stern J, Kim J, Wolf R, Lawler K, Kolson DL, Detre JA (2006) Caudate blood flow and volume are reduced in HIV+ neurocognitively impaired patients. Neurology 66:862–866

Anderson E, Zink W, Xiong H, Gendelman HE (2002) HIV-1-associated dementia: a metabolic encephalopathy perpetrated by virus-infected and immune-competent mononuclear phagocytes. J Acquir Immune Defic Syndr 31(suppl 2):S43–S54

Arendt G, Hefter H, Elsing C, Strohmeyer G, Freund HJ (1990) Motor dysfunctions in HIV-1 infected patients without clinically detectable central nervous system deficit. J Neurol 237:362–368

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

Aylward EH, Henderer JD, McArthur JC, Brettschneider PD, Harris GJ, Barta PE, Pearlson GD (1993) Reduced basal ganglia volume in HIV-1 associated dementia: results from quantitative neuroimaging. Neurology 43:2099–2104

Aylward EH, Brettschneider PD, McArthur JC, Harris GJ, Schlaepfer TE, Henderer JD, Barta PE, Tien AY, Pearlson GD (1995) Magnetic resonance imaging measurement of gray matter volume reductions in HIV dementia. Am J Psychiatry 152:987–994

Bagasra O, Lavi E, Bobroski L, Khalili K, Pestanner JP, Tawadros R, Pomerantz RJ (1996) Cellular reservoirs of HIV-1 in the CNS of infected individuals: identification by the combination of in situ polymerase chain reaction and immunohistochemistry. AIDS 10:573–585

Banks WA, Robinson SM, Wolf KM, Bess JW Jr, Arthur LO (2004) Binding, internalization, and membrane incorporation of human immunodeficiency virus -1 at the blood–brain barrier is differentially regulated. Neuroscience 128:143–153

Becker JT, Sanchez J, Dew MA, Lopez OL, Dorst SK, Banks G (1997) Neuropsychological abnormalities among HIV-infected individuals in a community-based sample. Neuropsychology 11(4):592–601

Benedict RHB (1997) Brief visuospatial memory test-revised. Psychological Assessment Resources, Odessa

Benton AL, Hamsher KD, Sivan AB (1994) Multilingual aphasia examination, 3rd edn. AJA Associates, Iowa City

Berger JR, Arendt G (2000) HIV dementia: the role of basal ganglia and dopaminergic systems. J Psychopharmacol 14:214–221

Berger JR, Kumar M, Kumar AM, Fernandez JB, Levin B (1994) Cerebrospinal fluid dopamine in HIV-1 infection. AIDS 8:67–71

Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson’s and Huntington: clinical and morphological and neurochemical correlations. J Neurol Sci 20:415–455

Bobardt MD, Salmon P, Wang L, Esko JD, Gabzuda D, Fiala M, Trono D, Van der Schueren B, David G, Gallay PA (2004) Contribution of proteoglycans to human immunodeficiency virus type-1 brain invasion. J Virol 78:6567–6584

Borozoski TJ, Brown RM, Rosvold HE, Goldman PS (1979) Cognitive deficits caused by regional depletion of dopamine in the prefrontal cortex of rhesus monkey. Science 205:929–932

Brabers NA, Nottet HS (2006) Role of the pro-inflammatory cytokines TNF-α and IL-1beta in HIV-associated dementia. Euro J Clin Invest 36:447–458

Brack-Werner R (1999) Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13(1):1–22

Broder CC, Dimitrov DS (1996) HIV and the 7-transmembrane domain receptors. Pathobiology 64:172–179

Butters N, Grant I, Haxby J, Judd LL, Martin A, McClelland J, Pequegnat W, Schacter D, Stover E (1990) Assessment of AIDS-related cognitive changes: recommendations of the NIMH workshop on neuropsychological assessment approaches. J Clin Exp Neuropsychol 12:963–978

Chang L, Ernst T, Leonido-Yee M, Witt M, Speck O, Walot I, Miller EN (1999) Highly active antiretroviral therapy reverses brain metabolite abnormalities in mild HIV dementia. Neurology 53:782–789

Chang L, Wang GJ, Volkow ND, Ernst T, Telang F, Logan J, Fowler JS (2008) Decreased brain dopamine transporters are related to cognitive deficits in HIV patients with or without cocaine abuse. NeuroImage 42(2):869–878

Cummings JL (1993) Frontal–subcortical circuits and human behavior. Arch Neurol 50:873–880

Dawes S, Suarez P, Casey CY, Cherner M, Marcotte TD, Letendre S, Grant I, Heaton RK, and the HNRC Group (2008) Variable patterns of neuropsychological performance in HIV-1 infection. J Clin Exp Neuropsychol 30(6):613–626

D’Esposito M, Defre JA, Alsop DC, Shin RK, Atlas S, Grassman M (1995) The neural basis of the central executive system of working memory. Nature 378:279–181

Di Rocco A, Bottiglieri T, Dorfman D, Werner P, Morrison C, Simpson D (2000) Decreased homovanillic acid in cerebrospinal fluid correlates with impaired neuropsychological function in HIV-1 infected patients. Clin Neuropharmacol 23(4):190–194

Ellis RJ, Hsia K, Spector SA, Nelson JA, Heaton RK, Wallace MR, Abramson I, Atkinson H, Grant I, McCutchan A, and the HIV Neurobehavioral Research Center Group (1997) Cerebrospinal fluid human immunodeficiency virus type 1 levels are elevated in neurocognitively impaired individuals with acquired immunodeficiency syndrome. Ann Neurol 42(5):679–688

Ellis RJ, Moore DJ, Childers MD, Letendre S, McCutchan JA, Wolfson T, Spector SA, Hsia K, Heaton RK, Grant I, for the HNRC Group (2002) Progression to neuropsychological impairment in human immunodeficiency virus infection predicted by elevated cerebrospinal fluid levels of human immunodeficiency virus RNA. Arch Neurol 59:923–928

Enting RH, Hoetelmans RM, Lamge JM, Burger DM, Beijnen JH, Portegies P (1998) Antiretroviral drugs and the central nervous system. AIDS 12:1941–1955

Everall IP, Heaton RK, Marcotte TD, Ellis RJ, McCutchan JA, Atkinson JH, Grant I, Mallory M, Masliah E (1999) Cortical synaptic density is reduced in mild to moderate human immunodeficiency virus neurocognitive disorder. HNRC Group. HIV Neurobiological Research Center. Brain Pathol 9:209–217

Fujimura RK, Goodkin K, Petito CK, Douyon R, Feaster DJ, Concha M, Shapshak P (1997) HIV-1 proviral DNA load across neuroanatomical regions of individuals with evidence for HIV-1 associated dementia. J Acquir Immun Defic Syndrome Hum Retrovirol 16:146–152

Gartner S (2000) HIV infection and dementia. Science 287(5453):602–604

Giovanni DG (2010) Editorial. Dopamine interaction with other neurotransmitter systems: relevance in the pathophysiology and treatment of CNS disorders. CNS Neurosci Therapeutics 16:125–126

Grahn JA, Parkinson JA, Owen AM (2009) The role of basal ganglia in learning and memory: neuropsychological studies. Behav Res 199:53–60

Grant I, Martin A (1994) Neurocognitive disorders associated with HIV infection. In: Grant I, Martin A (eds) Neuropsychology of HIV infection. Oxford University Press, New York, pp 3–20

Gronwall DMA (1977) Paced auditory serial addition task; a measure of recovery from concussion. Percept Mot Skills 44:367–373

Heaton RK, Grant I, Mathews CG (1991) Comprehensive norms for an expanded Halstead-Reitan Battery: demographic corrections. Research findings and clinical applications. Psychological Assessment Resources, Odessa

Heaton RK, Chelune GJ, Talley JL, Kay CG, Curtis G (1993) Wisconsin Card Sorting Test (WCST) manual-revised and expanded. Psychological Assessment Resources, Odessa

Heaton RK, Grant I, Butters N, White DA, Kirson D, Atkinson JH, McCutchan JA, Taylor MJ, Kelly MD, Ellis RJ (1995) The HNRC 500—neuropsychology of HIV infection at different disease stages. HIV Neurobehavioral Research Center. J Intl Neuropsychol Soc 1:231–251

Heyes MP, Brew BJ, Martin A, Price RW, Salazar AM, Sidtis JJ, Yergey JA, Mouradian MM, Sadler AE, Keilp J, Rubinow D, Markey SP (1991) Quinolinic acid in cerebrospinal fluid and serum in HIV-1 infection: relationship to clinical and neurological status. Ann Neurol 29(2):202–209

Ho D, Rota TR, Schooley RT, Kaplan JC, Allan JD, Groopman JE, Resnick L, Felsenstein D, Andrew CA, Hirsch MS (1985) Isolation of HTLV-III from cerebrospinal fluid and neural tissues of patients with neurologic syndromes related to the acquired immunodeficiency syndrome. N Engl J Med 313(24):1493–1497

Hollander H, Golden J, Mendelson T, Cortland D (1985) Extra pyramidal symptoms in AIDS patients given low-dose metoclopramide or chlorpromazine [letter]. Lancet 2:1186

Hornykiewicz O (1973) Dopamine in the basal ganglia: its role and therapeutic implications (including the clinical use of l-DOPA). Br Med Bull 29:172–178

Hornykiewicz O (1998) Biochemical aspects of Parkinson’s disease. Neurology 51(supplement 2):S2–S9

Hriso E, Kuhn T, Masdeu JC, Grundman M (1991) Extrapyramidal symptoms due to dopamine-blocking agents in patients with AIDS encephalopathy. Am J Psychiatry 148:1558–1561

Itoh K, Mehraein P, Weis S (2000) Neuronal damage of the substantia nigra in HIV-infected brains. Acta Neuropathol 99:376–384

Kaul M, Lipton SA (2006) Mechanisms of neuronal injury and death in HIV-1 associated dementia. Curr HIV Res 4:307–318

Kim RB, Fromm MF, Wandel C, Leake B, Wood JJ, Roden DM (1998) The drug transporter p-glycoprotein limits oral absorption and brain entry of HIV-1 protease inhibitors. J Clin Invest 101:289–294

Kolson DL, Lavie E, Gonzalez-Scarano F (1998) The effect of human immunodeficiency virus in the CNS. Adv Virus Res 50:1–47

Kramer-Hammerle S, Rothenaigner I, Wolf H, Bell JE, Brack-Werner R (2005) Cells of the nervous system as targets and reservoirs of the human immunodeficiency virus. Virus Res 111(2):194–213

Kumar AM, Borodowsky I, Fernandez B, Gonzalez L, Kumar M (2007) Human immunodeficiency virus type 1 RNA levels in different regions of human brain: quantification using real-time reverse transcriptase-polymerase chain reaction. J NeuroVirol 13:210–224

Kumar AM, Fernandez JB, Singer EJ, Commins D, Waldrop-Valverde D, Ownby RL, Kumar M (2009) Human immunodeficiency virus type-1 in the central nervous system leads to decreased dopamine in different regions of postmortem human brains. J NeuroVirol 15:257–274

Larsson M, Hagberg L, Forsman A, Norkrans G (1991) Cerebrospinal fluid catecholamines metabolites in HIV-1 infected patients. J Neurosci Res 28:406–409

Letendre S, Marquie-Beck J, Capparelli E, Best B, Clifford D, Collier AC, Gelman BB, McArthur JC, McCutchan JA, Morgello S, Simpson D, Grant I, Ellis RJ (2008) Validation of the CNS penetration—effectiveness rank for quantifying antiretroviral penetration into the central nervous system. Arch Neurol 65:65–70

Luciana M, Collins P, Depue RA (1998) Opposing roles for dopamine and serotonin in the modulation of human spatial working memory function. Cerebral Cortex 8:218–226

Marra CM, Zhao Y, Clifford DB, Letendre S, Evans S, Henry K, Ellid RJ, Rodriguez B, Coombs RW, Schiffito G, McArthur JC, Robertson K, AIDS Clinical Trials Group 736 Study Team (2009) Impact of combination antiretroviral therapy on cerebrospinal fluid HIV RNA and neurocognitive performance. AIDS 23(14):1909–1910

Masliah E, Achim CL, Ge N, DeTeresa R, Terry RD, Wiley CA (1992) Spectrum of HIV associated neocortical damage. Ann Neurol 32:85–93

Masliah E, Heaton RK, Marcotte TD, Ellis RJ, Wiley CA, Mallroy M, Achim CL, McCutcan JA, Nelson JA, Atkinson JH, Grant I (1997) Dendritic injury is a pathological substrate for human immunodeficiency virus related cognitive disorders. HNRC Group. The HIV Neurobehavioral Research Center. Ann Neurol 42:963–972

Mathews CG, Klove H (1964) Instruction manual for adult neuropsychology test battery. University of Wisconsin Medical School, Madison

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

McArthur J, Mclernen DR, Cronin MF, Nance-Sproson TE, Saah AJ, Clair MS, Lanier ER (1997) Relationship between human immunodeficiency virus associated dementia and viral load in cerebrospinal fluid and brain. Ann Neurol 42(5):689–698

McClernon DR, Lanier R, Gartner S, Feaser P, Pardo CA, St Claire M, Liao Q, McArthur JC (2001) HIV in the brain: RNA levels and patterns of zidovudine resistance. Neurology 57:1396–1401

Mirsattari SM, Power C, Nath A (1998) Parkinsonism with HIV infection. Mov Disord 13:684–689

Moore DJ, Masliah E, Rippeth JD, Gonzalez R, Carey CL, Cherner M, Ellis RJ, Achim CL, Marcotte TD, Heaton RK, Grant R, and the HNRC Group (2005) Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS 20:879–887

Morgello S, Gelman BB, Kozlowski PB, Vinters HV, Masliah E, Cornford M, Cavert W, Marra C, Grant I, Singer EJ (2001) The National NeuroAIDS Tissue Consortium: a new paradigm in brain banking with an emphasis on infectious diseases. Neuropathol Appl Neurobiol 27:326–335

Nath A (2002) Human immunodeficiency virus proteins in neuropathogenesis of HIV dementia. J Infect Dis 186(Suppl 2):S193–S198

Nath A, Geiger J (1998) Neurobiological aspects of human immunodeficiency virus infection: neurotoxic mechanisms. Prog Neurobiol 54:19–33

Nath A, Jones M, Maragos W, Booz R, Mactutus C, Bell J, Hauser K, Mattson M (2000) Neurotoxicity and dysfunction of dopaminergic systems associated with AIDS dementia. J Psychopharmacol 14(3):222–228

Navia BA, Jordan BD, Price RW (1986) The AIDS dementia complex: clinical features. Ann Neurol 19:517–524

Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53–83

Nottet HS, Pesidsky Y, Sasseville VG, Nukuma AN, Bock P, Zhai QH, Sharer LR, McComb RD, Swindells S, Soderland C, Gendelman HE (1996) Mechanisms for the transendothelial migration of HIV-1 infected monocytes in to the brain. J Immunol 156:1284–1295

Obermann M, Kuper M, Kastrup O, Yaldizli O, Esser S, Thiermann J, Koutsilieri E, Arendt G, Diener HC, Maschke M (2009) Substantia nigra hyperechogenicity and CSF dopamine depletion in HIV. J Neurol 256:948–953

Owen AM, Doyon J, Petrides M, Evans AC (1996) Planning and spatial working memory: a positron emission tomography study in humans. Eur J Neurosci 8:353–364

Peavy G, Jacobs D, Salmon DP (1994) Verbal memory performance of patients with human immunodeficiency virus infection: evidence of subcortical dysfunction. J Clin Exp Neuropsychol 16:508–523

Pomara N, Crandall DT, Choi SJ, Johnson G, Lim KO (2001) White matter abnormalities in HIV-1 infection: a diffusion tensor imaging study. Psychiatry Res 106:15–24

Previc FH (1999) Dopamine and origin of human intelligence. Brain Cognition 41:299–350

Rajput AH, Sitte HH, Rajput A, Fenton ME, Pifi C, Hornykiewicz O (2008) Globus pallidus dopamine and Parkinson motor subtypes: clinical and brain biochemical correlations. Neurology 17(16 pt 2):1403–1410

Reger M, Welsh R, Razani J, Martin DJ, Boon KB (2002) A meta-analysis of the neuropsychological sequelae of HIV-1 infection. J Int Neuropsychol Soc 8:410–424

Resnick L, Berger JR, Shapshak P, Tourtellote WW (1988) Early penetration of the blood brain–barrier by HIV. Neurology 38:9–14

Reyes MG, Faraldi F, Senseng CS, Flowers C, Fariello R (1991) Nigral degeneration in acquired immune deficiency syndrome (AIDS). Acta Neuropathol 82:39–44

Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, McArthur JC, Collier AC, Evans SR, Ellis RJ (2007) The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 21:1915–1921

Sacktor N (2002) The epidemiology of human immunodeficiency virus-associated neurological disease in era of highly active antiretroviral therapy. J NeuroVirol 8(Suppl 2):115–121

Sacktor N, McDermott MP, Marder K, Schiffito G, Selnes OA, McArthur JC, Stern Y, Albert S, Palumbo D, Kieburtz A, 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

Sardar AM, Czudek C, Reynolds GP (1996) Dopamine deficits in the brain: the neurochemical basis of Parkinsonian symptoms in AIDS. Neuroreport 7:910–912

Schrager LK, D’Souza MP (1998) Cellular and anatomical reservoirs of HIV-1 in patients receiving potent antiretroviral combination therapy. JAMA 280:67–71

Tracey I, Carr CA, Guimaraes AR, Worth JL, Navia BA, Gonzalez RG (1996) Brain choline-containing compounds are elevated in HIV-positive patients before the onset of AIDS dementia complex. A proton magnetic resonance spectroscopy study. Neurology 46(3):783–788

Tracey I, Hamberg LM, Guimaraes AR, Hunter G, Chang I, Navia BA, Gonzalez RG (1998) Increased cerebral blood volume in HIV-positive patients detected by functional MRI. Neurology 50:1821–1826

Van Kammen DP, Van Kammen WB, Mann LS, Seppala T, Linnoila M (1986) Dopamine metabolism in cerebrospinal fluid of drug free schizophrenic patients with and without cortical atrophy. Arch Gen Psychiatry 43:978–983

Walsh FX, Stevens JT, Langlais PJ, Bird ED (1982) Dopamine and homovanillic acid concentrations in striatal and limbic regions of human brain. Ann Neurol 12:52–55

Wang GJ, Chang L, Volkow ND, Telang F, Logan J, Ernst T, Fowler JS (2004) Decreased brain dopaminergic transporters in HIV-associated dementia patients. Brain 127:2452–2458

Wechsler D (1997) The Wechsler adult intelligent scale-III edition. Psychological Corp, New York

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

Wilk S, Stanley M (1978) Dopamine metabolites in human brain tissue. J Neural Transm 39:281–290

Wilkie FI, Goodkin K, van Zulien MH, Tyll MD, Lecusay R, Edwin T (2000) Cognitive effects of HIV-1 infection. CNS Spectrum 5(5):33–51

Woods SP, Moore DJ, Weber E, Grant I (2009) Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychol Rev 19:152–168