Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T18:58:07.523Z Has data issue: false hasContentIssue false

Prepulse Inhibition in HIV-Associated Neurocognitive Disorders

Published online by Cambridge University Press:  03 April 2013

Arpi Minassian*
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California Center of Excellence for Stress and Mental Health (CESAMH), Veteran's Administration, San Diego, California
Brook L. Henry
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California
Steven Paul Woods
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California
Florin Vaida
Affiliation:
Division of Biostatistics and Bioinformatics, Department of Family and Preventative Medicine, University of California San Diego, La Jolla, California
Igor Grant
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California
Mark A. Geyer
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California VA San Diego Healthcare System, San Diego, California
William Perry
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California
*
Correspondence and reprint requests to: Arpi Minassian, UCSD Department of Psychiatry, 200 West Arbor Drive, Mailcode 8620, San Diego, CA 92103-8620. E-mail: [email protected]

Abstract

Sensorimotor inhibition, or the ability to filter out excessive or irrelevant information, theoretically supports a variety of higher-level cognitive functions. Impaired inhibition may be associated with increased impulsive and risky behavior in everyday life. Individuals infected with HIV frequently show impairment on tests of neurocognitive function, but sensorimotor inhibition in this population has not been studied and may be a contributor to the profile of HIV-associated neurocognitive disorders (HAND). Thirty-seven HIV-infected individuals (15 with HAND) and 48 non-infected comparison subjects were assessed for prepulse inhibition (PPI), an eyeblink startle paradigm measuring sensorimotor gating. Although HIV status alone was not associated with PPI deficits, HIV-positive participants meeting criteria for HAND showed impaired PPI compared to cognitively intact HIV-positive subjects. In HIV-positive subjects, PPI was correlated with working memory but was not associated with antiretroviral therapy or illness factors. In conclusion, sensorimotor disinhibition in HIV accompanies deficits in higher-order cognitive functions, although the causal direction of this relationship requires investigation. Subsequent research on the role of sensorimotor gating on decision-making and risk behaviors in HIV may be indicated. (JINS, 2013, 19, 1–9)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmari, S.E., Risbrough, V.B., Geyer, M.A., Simpson, H.B. (2012). Impaired sensorimotor gating in unmedicated adults with obsessive-compulsive disorder. Neuropsychopharmacology, 37(5), 12161223.CrossRefGoogle ScholarPubMed
Antinori, A., Arendt, G., Becker, J.T., Brew, B.J., Byrd, D.A., Cherner, M., Wojna, V.E. (2007). Updated research nosology for HIV-associated neurocognitive disorders. Neurology, 69(18), 17891799.CrossRefGoogle ScholarPubMed
Bitsios, P., Giakoumaki, S.G., Theou, K., Frangou, S. (2006). Increased prepulse inhibition of the acoustic startle response is associated with better strategy formation and execution times in healthy males. Neuropsychologia, 44(12), 24942499.CrossRefGoogle ScholarPubMed
Blackstone, K., Moore, D.J., Franklin, D.R., Clifford, D.B., Collier, A.C., Marra, C.M., Heaton, R.K. (2012). Defining neurocognitive impairment in HIV: Deficit scores versus clinical ratings. Clinical Neuropsychology, 26(6), 894908.CrossRefGoogle ScholarPubMed
Braff, D.L., Geyer, M.A. (1990). Sensorimotor gating and schizophrenia. Human and animal model studies. Archives of General Psychiatry, 47(2), 181188.CrossRefGoogle ScholarPubMed
Braff, D.L., Geyer, M.A., Swerdlow, N.R. (2001). Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl), 156(2–3), 234258.CrossRefGoogle ScholarPubMed
Braff, D.L., Grillon, C., Geyer, M.A. (1992). Gating and habituation of the startle reflex in schizophrenic patients. Archives of General Psychiatry, 49(3), 206215.CrossRefGoogle ScholarPubMed
Butler, R.W., Jenkins, M.A., Sprock, J., Braff, D.L. (1992). Wisconsin Card Sorting Test deficits in chronic paranoid schizophrenia: Evidence for a relatively discrete subgroup? Schizophrenia Research, 7(2), 169176.CrossRefGoogle ScholarPubMed
Carey, C.L., Woods, S.P., Gonzalez, R., Conover, E., Marcotte, T.D., Grant, I., Heaton, R.K. (2004). Predictive validity of global deficit scores in detecting neuropsychological impairment in HIV infection. Journal of Clinical and Experimental Neuropsychology, 26(3), 307319.CrossRefGoogle ScholarPubMed
Chang, L., Ernst, T., Witt, M.D., Ames, N., Gaiefsky, M., Miller, E. (2002). Relationships among brain metabolites, cognitive function, and viral loads in antiretroviral-naive HIV patients. Neuroimage, 17(3), 16381648.CrossRefGoogle ScholarPubMed
Chao, L.L., Lindgren, J.A., Flenniken, D.L., Weiner, M.W. (2004). ERP evidence of impaired central nervous system function in virally suppressed HIV patients on antiretroviral therapy. Clinical Neurophysiology, 115(7), 15831591.CrossRefGoogle ScholarPubMed
Chung, A., Lyoo, I.K., Kim, S.J., Hwang, J., Bae, S.C., Sung, Y.H., Renshaw, P.F. (2007). Decreased frontal white-matter integrity in abstinent methamphetamine abusers. International Journal of Neuropsychopharmacology, 10(6), 765775.CrossRefGoogle ScholarPubMed
Csomor, P.A., Stadler, R.R., Feldon, J., Yee, B.K., Geyer, M.A., Vollenweider, F.X. (2008). Haloperidol differentially modulates prepulse inhibition and p50 suppression in healthy humans stratified for low and high gating levels. Neuropsychopharmacology, 33(3), 497512.CrossRefGoogle ScholarPubMed
Deutsch, R., Ellis, R.J., McCutchan, J.A., Marcotte, T.D., Letendre, S., Grant, I. (2001). AIDS-associated mild neurocognitive impairment is delayed in the era of highly active antiretroviral therapy. Aids, 15(14), 18981899.CrossRefGoogle ScholarPubMed
Dore, G.J., Cooper, D.A., Barrett, C., Goh, L.E., Thakrar, B., Atkins, M. (1999). Dual efficacy of lamivudine treatment in human immunodeficiency virus/hepatitis B virus-coinfected persons in a randomized, controlled study (CAESAR). The CAESAR Coordinating Committee. The Journal of Infectious Diseases, 180(3), 607613.CrossRefGoogle Scholar
Feifel, D., Minassian, A., Perry, W. (2009). Prepulse inhibition of startle in adults with ADHD. Journal of Psychiatric Research, 43(4), 484489.CrossRefGoogle ScholarPubMed
Fein, G., Biggins, C.A., MacKay, S. (1995). Delayed latency of the event-related brain potential P3A component in HIV disease. Progressive effects with increasing cognitive impairment. Archives of Neurology, 52(11), 11091118.CrossRefGoogle ScholarPubMed
Geyer, M.A. (2006). Are cross-species measures of sensorimotor gating useful for the discovery of procognitive cotreatments for schizophrenia? Dialogues in Clinical Neuroscience, 8(1), 916.CrossRefGoogle ScholarPubMed
Geyer, M.A., Krebs-Thomson, K., Braff, D.L., Swerdlow, N.R. (2001). Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: A decade in review. Psychopharmacology (Berl), 156(2–3), 117154.CrossRefGoogle ScholarPubMed
Giakoumaki, S.G., Bitsios, P., Frangou, S. (2006). The level of prepulse inhibition in healthy individuals may index cortical modulation of early information processing. Brain Research, 1078(1), 168170.CrossRefGoogle ScholarPubMed
Hardy, D.J., Castellon, S.A., Hinkin, C.H., Levine, A.J., Lam, M.N. (2008). Sensation seeking and visual selective attention in adults with HIV/AIDS. AIDS and Behavior, 12(6), 930934.CrossRefGoogle ScholarPubMed
Hasenkamp, W., Kelley, M., Egan, G., Green, A., Wilcox, L., Boshoven, W., Duncan, E. (2011). Lack of relationship between acoustic startle and cognitive variables in schizophrenia and control subjects. Psychiatry Research, 187(3), 324328.CrossRefGoogle ScholarPubMed
Heaton, R.K., Clifford, D.B., Franklin, D.R. Jr., Woods, S.P., Ake, C., Vaida, F., Grant, I. (2010). HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology, 75(23), 20872096.CrossRefGoogle ScholarPubMed
Heaton, R.K., Franklin, D.R., Ellis, R.J., McCutchan, J.A., Letendre, S.L., Leblanc, S., Grant, I. (2011). HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. Journal of Neurovirology, 17(1), 316.CrossRefGoogle ScholarPubMed
Heaton, R.K., Grant, I., Butters, N., White, D.A., Kirson, D., Atkinson, J.H., Abramson, I. (1995). The HNRC 500--neuropsychology of HIV infection at different disease stages. HIV Neurobehavioral Research Center. Journal of the International Neuropsychological Society, 1(3), 231251.CrossRefGoogle ScholarPubMed
Hinkin, C.H., Castellon, S.A., Hardy, D.J., Granholm, E., Siegle, G. (1999). Computerized and traditional stroop task dysfunction in HIV-1 infection. Neuropsychology, 13(2), 306316.CrossRefGoogle ScholarPubMed
Hofmann, W., Schmeichel, B.J., Baddeley, A.D. (2012). Executive functions and self-regulation. Trends in Cognitive Sciences, 16(3), 174180.CrossRefGoogle ScholarPubMed
Joska, J.A., Westgarth-Taylor, J., Hoare, J., Thomas, K.G., Paul, R., Myer, L., Stein, D.J. (2012). Neuropsychological outcomes in adults commencing highly active anti-retroviral treatment in South Africa: A prospective study. BMC Infectious Diseases, 12, 39.CrossRefGoogle ScholarPubMed
Kamat, R., Woods, S.P., Marcotte, T.D., Ellis, R.J., Grant, I. (2012). Implications of apathy for everyday functioning outcomes in persons living with HIV infection. Archives of Clinical Neuropsychology, 27(5), 520531.CrossRefGoogle ScholarPubMed
Kedzior, K.K., Martin-Iverson, M.T. (2006). Chronic cannabis use is associated with attention-modulated reduction in prepulse inhibition of the startle reflex in healthy humans. Journal of Psychopharmacology, 20(4), 471484.CrossRefGoogle ScholarPubMed
Kedzior, K.K., Martin-Iverson, M.T. (2007). Attention-dependent reduction in prepulse inhibition of the startle reflex in cannabis users and schizophrenia patients--a pilot study. European Journal of Pharmacology, 560(2–3), 176182.CrossRefGoogle ScholarPubMed
Kishi, T., Fukuo, Y., Okochi, T., Kawashima, K., Moriwaki, M., Furukawa, O., Iwata, N. (2012). The relationship between acoustic startle response measures and cognitive functions in Japanese patients with schizophrenia. Neuromolecular Medicine, 14(2), 131138.CrossRefGoogle ScholarPubMed
Koch, M. (1998). Sensorimotor gating changes across the estrous cycle in female rats. Physiology and Behavior, 64(5), 625628.CrossRefGoogle ScholarPubMed
Letendre, S.L., McCutchan, J.A., Childers, M.E., Woods, S.P., Lazzaretto, D., Heaton, R.K., Ellis, R.J. (2004). Enhancing antiretroviral therapy for human immunodeficiency virus cognitive disorders. Annals of Neurology, 56(3), 416423.CrossRefGoogle ScholarPubMed
Letendre, S.L., Woods, S.P., Ellis, R.J., Atkinson, J.H., Masliah, E., van den Brande, G., Everall, I. (2006). Lithium improves HIV-associated neurocognitive impairment. Aids, 20(14), 18851888.CrossRefGoogle ScholarPubMed
Martin, E.M., Novak, R.M., Fendrich, M., Vassileva, J., Gonzalez, R., Grbesic, S., Sworowski, L. (2004). Stroop performance in drug users classified by HIV and hepatitis C virus serostatus. Journal of the International Neuropsychological Society, 10(2), 298300.CrossRefGoogle ScholarPubMed
Martin, H.P. (1995). Mild cognitive impairment in HIV disease. Nurse Practitioner, 20(8), 9497.CrossRefGoogle ScholarPubMed
Maschke, M., Kastrup, O., Esser, S., Ross, B., Hengge, U., Hufnagel, A. (2000). Incidence and prevalence of neurological disorders associated with HIV since the introduction of highly active antiretroviral therapy (HAART). Journal of Neurology, Neurosurgery, and Psychiatry, 69(3), 376380.CrossRefGoogle ScholarPubMed
Mathias, C.W., Blumenthal, T.D., Dawes, M.A., Liguori, A., Richard, D.M., Bray, B., Dougherty, D.M. (2012). Failure to sustain prepulse inhibition in adolescent marijuana users. Drug and Alcohol Dependence, 116(1–3), 110116.CrossRefGoogle Scholar
Minassian, A., Feifel, D., Perry, W. (2007). The relationship between sensorimotor gating and clinical improvement in acutely ill schizophrenia patients. Schizophrenia Research, 89(1–3), 225231.CrossRefGoogle ScholarPubMed
Molina, V., Cortes, B., Perez, J., Martin, C., Villa, R., Lopez, D.E., Sancho, C. (2010). No association between prepulse inhibition of the startle reflex and neuropsychological deficit in chronic schizophrenia. European Archives of Psychiatry and Clinical Neurosciences, 260(8), 609615.CrossRefGoogle ScholarPubMed
Moore, D.J., Arce, M., Moseley, S., McCutchan, J.A., Marquie-Beck, J., Franklin, D.R., Grant, I. (2011). Family history of dementia predicts worse neuropsychological functioning among HIV-infected persons. The Journal of Neuropsychiatry and Clinical Neurosciences, 23(3), 316323.CrossRefGoogle ScholarPubMed
Overton, E.T., Kauwe, J.S., Paul, R., Tashima, K., Tate, D.F., Patel, P., Clifford, D.B. (2012). Performances on the CogState and standard neuropsychological batteries among HIV patients without dementia. AIDS and Behavior, 15(8), 19021909.CrossRefGoogle Scholar
Perry, W., Feifel, D., Minassian, A., Bhattacharjie, I., Braff, D.L. (2002). Information processing deficits in acutely psychotic schizophrenia patients medicated and unmedicated at the time of admission. The American Journal of Psychiatry, 159(8), 13751381.CrossRefGoogle ScholarPubMed
Perry, W., Minassian, A., Feifel, D., Braff, D.L. (2001). Sensorimotor gating deficits in bipolar disorder patients with acute psychotic mania. Biological Psychiatry, 50(6), 418424.CrossRefGoogle ScholarPubMed
Pistell, P.J., Gupta, S., Knight, A.G., Domingue, M., Uranga, R.M., Ingram, D.K., Bruce-Keller, A.J. (2010). Metabolic and neurologic consequences of chronic lopinavir/ritonavir administration to C57BL/6 mice. Antiviral Research, 88(3), 334342.CrossRefGoogle ScholarPubMed
Polich, J., Ilan, A., Poceta, J.S., Mitler, M.M., Darko, D.F. (2000). Neuroelectric assessment of HIV: EEG, ERP, and viral load. International Journal of Psychophysiology, 38(1), 97108.CrossRefGoogle ScholarPubMed
Rabin, R.A., Sacco, K.A., George, T.P. (2009). Correlation of prepulse inhibition and Wisconsin Card Sorting Test in schizophrenia and controls: Effects of smoking status. Schizophrenia Research, 114(1–3), 9197.CrossRefGoogle ScholarPubMed
Rippeth, J.D., Heaton, R.K., Carey, C.L., Marcotte, T.D., Moore, D.J., Gonzalez, R., Grant, I. (2004). Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. Journal of the International Neuropsychological Society, 10(1), 114.CrossRefGoogle ScholarPubMed
Sacktor, N., Lyles, R.H., Skolasky, R., Kleeberger, C., Selnes, O.A., Miller, E.N., McArthur, J.C. (2001). HIV-associated neurologic disease incidence changes: Multicenter AIDS Cohort Study, 1990–1998. Neurology, 56(2), 257260.CrossRefGoogle ScholarPubMed
Sacktor, N., McDermott, M.P., Marder, K., Schifitto, G., Selnes, O.A., McArthur, J.C., Epstein, L. (2002). HIV-associated cognitive impairment before and after the advent of combination therapy. Journal of Neurovirology, 8(2), 136142.CrossRefGoogle ScholarPubMed
Semple, S.J., Zians, J., Grant, I., Patterson, T.L. (2006). Methamphetamine use, impulsivity, and sexual risk behavior among HIV-positive men who have sex with men. Journal of Addictive Diseases, 25(4), 105114.CrossRefGoogle ScholarPubMed
Sun, B., Abadjian, L., Rempel, H., Monto, A., Pulliam, L. (2013). Differential Cognitive impairment in HCV coinfected men with controlled HIV compared to HCV monoinfection. Journal of Acquired Immune Deficiency Syndromes, 62(2), 190196.CrossRefGoogle ScholarPubMed
Swerdlow, N.R. (1996). Cortico-striatal substrates of cognitive, motor and sensory gating: Speculations and implications for psychological function and dysfunction. In J. Panksepp (Ed.), Advances in biological psychiatry (Vol. 2, pp. 179208). Greenwich, CT: JAI Press Inc.Google Scholar
Swerdlow, N.R., Benbow, C.H., Zisook, S., Geyer, M.A. (1993). A preliminary assessment of sensorimotor gating in patients with obsessive compulsive disorder. Biological Psychiatry, 33(4), 298301.CrossRefGoogle ScholarPubMed
Swerdlow, N.R., Hartman, P.L., Auerbach, P.P. (1997). Changes in sensorimotor inhibition across the menstrual cycle: Implications for neuropsychiatric disorders. Biological Psychiatry, 41(4), 452460.CrossRefGoogle ScholarPubMed
Swerdlow, N.R., Light, G.A., Cadenhead, K.S., Sprock, J., Hsieh, M.H., Braff, D.L. (2006). Startle gating deficits in a large cohort of patients with schizophrenia: Relationship to medications, symptoms, neurocognition, and level of function. Archives of General Psychiatry, 63(12), 13251335.CrossRefGoogle Scholar
Swerdlow, N.R., Paulsen, J., Braff, D.L., Butters, N. (1995). Impaired prepulse inhibition of acoustic and tactile startle response in patients with Huntington's disease. Journal of Neurology, Neurosurgery, and Psychiatry, 58(2), 192200.CrossRefGoogle ScholarPubMed
Zeger, S.L., Liang, K.Y. (1986). Longitudinal data analysis for discrete and continuous outcomes. Biometrics, 42(1), 121130.CrossRefGoogle ScholarPubMed