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Facial emotion recognition impairments in individuals with HIV

Published online by Cambridge University Press:  20 October 2010

URAINA S. CLARK*
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island
RONALD A. COHEN
Affiliation:
Department of Psychiatry and Human Behavior, The Warren Alpert Medical School of Brown University, Providence, Rhode Island Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island
MICHELLE L. WESTBROOK
Affiliation:
Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island Center for AIDS Research, The Miriam Hospital, Providence, Rhode Island
KATHRYN N. DEVLIN
Affiliation:
Centers for Behavioral and Preventive Medicine, The Miriam Hospital, Providence, Rhode Island
KAREN T. TASHIMA
Affiliation:
Center for AIDS Research, The Miriam Hospital, Providence, Rhode Island Department of Medicine, The Warren Alpert Medical School of Brown University, Providence, Rhode Island
*
*Correspondence and reprint requests to: Uraina Clark, Ph.D., Centers for Behavioral & Preventative Medicine, The CORO Building, Suite 500, 1 Hoppin Street, Providence, Rhode Island 02903. E-mail: Uraina_Clark@brown.edu

Abstract

Characterized by frontostriatal dysfunction, human immunodeficiency virus (HIV) is associated with cognitive and psychiatric abnormalities. Several studies have noted impaired facial emotion recognition abilities in patient populations that demonstrate frontostriatal dysfunction; however, facial emotion recognition abilities have not been systematically examined in HIV patients. The current study investigated facial emotion recognition in 50 nondemented HIV-seropositive adults and 50 control participants relative to their performance on a nonemotional landscape categorization control task. We examined the relation of HIV-disease factors (nadir and current CD4 levels) to emotion recognition abilities and assessed the psychosocial impact of emotion recognition abnormalities. Compared to control participants, HIV patients performed normally on the control task but demonstrated significant impairments in facial emotion recognition, specifically for fear. HIV patients reported greater psychosocial impairments, which correlated with increased emotion recognition difficulties. Lower current CD4 counts were associated with poorer anger recognition. In summary, our results indicate that chronic HIV infection may contribute to emotion processing problems among HIV patients. We suggest that disruptions of frontostriatal structures and their connections with cortico-limbic networks may contribute to emotion recognition abnormalities in HIV. Our findings also highlight the significant psychosocial impact that emotion recognition abnormalities have on individuals with HIV. (JINS, 2010, 16, 1127–1137.)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2010

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References

REFERENCES

Adolphs, R. (2002a). Neural systems for recognizing emotion. Current opinion in neurobiology, 12(2), 169177.CrossRefGoogle ScholarPubMed
Adolphs, R. (2002b). Recognizing emotion from facial expressions: Psychological and neurological mechanisms. Behavioral and Cognitive Neuroscience Reviews, 1(1), 2162.CrossRefGoogle ScholarPubMed
Alexander, G.E., Crutcher, M.D., & DeLong, M.R. (1990). Basal ganglia-thalamocortical circuits: Parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Progress in Brain Research, 85, 119146.CrossRefGoogle ScholarPubMed
Ances, B.M., Roc, A.C., Wang, J., Korczykowski, M., Okawa, J., Stern, J., Kim, J., Wolf, R., Lawler, K., Kolson, D.L., & Detre, J.A. (2006). Caudate blood flow and volume are reduced in HIV+ neurocognitively impaired patients. Neurology, 66(6), 862866.CrossRefGoogle ScholarPubMed
Aylward, E.H., Henderer, J.D., McArthur, J.C., Brettschneider, P.D., Harris, G.J., Barta, P.E., & Pearlson, G.D. (1993). Reduced basal ganglia volume in HIV-1-associated dementia: Results from quantitative neuroimaging. Neurology, 43, 20992104.CrossRefGoogle ScholarPubMed
Benton, A.L., Sivan, A.B., Hamsher, K.S., Varney, N.R., & Spreen, O. (1994). Contributions to neuropsychological assessment: A clinical manual (2nd ed.). New York: Oxford University Press.Google Scholar
Bing, E.G., Burnam, M.A., Longshore, D., Fleishman, J.A., Sherbourne, C.D., London, A.S., Turner, B.J., Eggan, F., Beckman, R., Vitiello, B., Morton, S.C., Orlando, M., Bozzette, S.A., Ortiz-Barron, L., & Shapiro, M. (2001). Psychiatric disorders and drug use among human immunodeficiency virus-infected adults in the United States. Archives of General Psychiatry, 58(8), 721728.CrossRefGoogle ScholarPubMed
Calder, A.J., Keane, J., Manly, T., Sprengelmeyer, R., Scott, S., Nimmo-Smith, I., & Young, A.W. (2003). Facial expression recognition across the adult life span. Neuropsychologia, 41(2), 195202.CrossRefGoogle ScholarPubMed
Calder, A.J., Lawrence, A.D., & Young, A.W. (2001). Neuropsychology of fear and loathing. Nature Reviews. Neuroscience, 2(5), 352363.CrossRefGoogle Scholar
Cardenas, V., Meyerhoff, D., Studholme, C., Kornak, J., Rothlind, J., Lampiris, H., Neuhaus, J., Grant, R., Chao, L., Truran, D., & Weiner, M. (2009). Evidence for ongoing brain injury in human immunodeficiency virus-positive patients treated with antiretroviral therapy. Journal of Neurovirology, 15(4), 324333.CrossRefGoogle ScholarPubMed
Childs, E.A., Lyles, R.H., Selnes, O.A., Chen, B., Miller, E.N., Cohen, B.A., Becker, J.T., Mellors, J., & McArthur, J.C. (1999). Plasma viral load and CD4 lymphocytes predict HIV-associated dementia and sensory neuropathy. Neurology, 52(3), 607613.CrossRefGoogle ScholarPubMed
Ciesla, J.A., & Roberts, J.E. (2001). Meta-analysis of the relationship between HIV infection and risk for depressive disorders. American Journal of Psychiatry, 158(5), 725730.CrossRefGoogle ScholarPubMed
Clark, U.S., Neargarder, S., & Cronin-Golomb, A. (2008). Specific impairments in the recognition of emotional facial expressions in Parkinson’s disease. Neuropsychologia, 46(9), 23002309.CrossRefGoogle ScholarPubMed
Clark, U.S., Oscar-Berman, M., Shagrin, B., & Pencina, M. (2007). Alcoholism and judgments of affective stimuli. Neuropsychology, 21(3), 346362.CrossRefGoogle ScholarPubMed
Cohen, R.A., Harezlak, J., Schifitto, G., Hana, G., Clark, U., Gongvatana, A., Paul, R., Taylor, M., Thompson, P., Alger, J., Brown, M., Zhong, J., Campbell, T., Singer, E., Daar, E., McMahon, D., Tso, Y., Yiannoutsos, C.T., & Navia, B. (2010). Effects of nadir CD4 count and duration of human immunodeficiency virus infection on brain volumes in the highly active antiretroviral therapy era. Journal of Neurovirology, 16(1), 2532.CrossRefGoogle ScholarPubMed
Cysique, L.A., Maruff, P., & Brew, B.J. (2006). Variable benefit in neuropsychological function in HIV-infected HAART-treated patients. Neurology, 66(9), 14471450.CrossRefGoogle ScholarPubMed
Darwin, C. (1872/1965). The expression of the emotions in man and animals. Chicago: University of Chicago Press.CrossRefGoogle Scholar
Davidson, R.J. (1993). Parsing affective space: Perspectives from neuropsychology and psychophysiology. Neuropsychology, 7(4), 464475.CrossRefGoogle Scholar
Derntl, B., Habel, U., Robinson, S., Windischberger, C., Kryspin-Exner, I., Gur, R.C., & Moser, E. (2009). Amygdala activation during recognition of emotions in a foreign ethnic group is associated with duration of stay. Social Neuroscience, 4(4), 294307.CrossRefGoogle Scholar
Dujardin, K., Blairy, S., Defebvre, L., Duhem, S., Noel, Y., Hess, U., & Destee, A. (2004). Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia, 42(2), 239250.CrossRefGoogle ScholarPubMed
Ekman, P., & Friesen, W.V. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Elfenbein, H.A., & Ambady, N. (2003). When familiarity breeds accuracy: Cultural exposure and facial emotion recognition. Journal of Personality and Social Psychology, 85(2), 276290.CrossRefGoogle ScholarPubMed
Falkum, E., & Vaglum, P. (2005). The relationship between interpersonal problems and occupational stress in physicians. General Hospital Psychiatry, 27(4), 285291.CrossRefGoogle ScholarPubMed
Feinberg, T.E., Rifkin, A., Schaffer, C., & Walker, E. (1986). Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Psychiatry, 43(3), 276279.CrossRefGoogle ScholarPubMed
Ferrando, S.J., Rabkin, J.G., van Gorp, W., Lin, S.H., & McElhiney, M. (2003). Longitudinal improvement in psychomotor processing speed is associated with potent combination antiretroviral therapy in HIV-1 infection. Journal of Neuropsychiatry and Clinical Neurosciences, 15(2), 208214.CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189198.CrossRefGoogle Scholar
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., Benedetti, F., Abbamonte, M., Gasparotti, R., Barale, F., Perez, J., McGuire, P., & Politi, P. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience, 34(6), 418432.Google ScholarPubMed
Gonzalez-Scarano, F., & Martin-Garcia, J. (2005). The neuropathogenesis of AIDS. Nature Reviews. Immunology, 5(1), 6981.CrossRefGoogle ScholarPubMed
Han, J.S., McMahan, R.W., Holland, P., & Gallagher, M. (1997). The role of an amygdalo-nigrostriatal pathway in associative learning. Journal of Neuroscience, 17(10), 39133919.CrossRefGoogle ScholarPubMed
Hinkin, C.H., Castellon, S.A., Atkinson, J.H., & Goodkin, K. (2001). Neuropsychiatric aspects of HIV infection among older adults. Journal of Clinical Epidemiology, 54 Suppl. 1, S4452.CrossRefGoogle ScholarPubMed
Horowitz, L.M., Alden, L.E., Wiggins, J.S., & Pincus, A.L. (2000). IIP–64/IIP–32 professional manual. San Antonio, TX: Psychological Corporation.Google Scholar
Horowitz, L.M., Rosenberg, S.E., Baer, B.A., Ureno, G., & Villasenor, V.S. (1988). Inventory of interpersonal problems: Psychometric properties and clinical applications. Journal of Consulting and Clinical Psychology, 56(6), 885892.CrossRefGoogle ScholarPubMed
Jernigan, T.L., Archibald, S., Hesselink, J.R., Atkinson, J.H., Velin, R.A., McCutchan, J.A., Chandler, J., & Grant, I. (1993). Magnetic resonance imaging morphometric analysis of cerebral volume loss in human immunodeficiency virus infection. The HNRC Group. Archives of Neurology, 50(3), 250255.CrossRefGoogle ScholarPubMed
Johnson, S.A., Stout, J.C., Solomon, A.C., Langbehn, D.R., Aylward, E.H., Cruce, C.B., Ross, C.A., Nance, M., Kayson, E., Julian-Baros, E., Hayden, M.R., Kieburtz, K., Guttman, M., Oakes, D., Shoulson, I., Beglinger, L., Duff, K., Penziner, E., & Paulsen, J.S. (2007). Beyond disgust: Impaired recognition of negative emotions prior to diagnosis in Huntington’s disease. Brain, 130(Pt. 7), 17321744.CrossRefGoogle ScholarPubMed
Kellogg, S.H., McHugh, P.F., Bell, K., Schluger, J.H., Schluger, R.P., LaForge, K.S., Ho, A., & Kreek, M.J. (2003). The Kreek-McHugh-Schluger-Kellogg scale: A new, rapid method for quantifying substance abuse and its possible applications. Drug and Alcohol Dependence, 69(2), 137150.CrossRefGoogle Scholar
Kelly, R.M., & Strick, P.L. (2004). Macro-architecture of basal ganglia loops with the cerebral cortex: Use of rabies virus to reveal multisynaptic circuits. Progress in Brain Research, 143, 449459.Google ScholarPubMed
Kornreich, C., Foisy, M.L., Philippot, P., Dan, B., Tecco, J., Noel, X., Hess, U., Pelc, I., & Verbanck, P. (2003). Impaired emotional facial expression recognition in alcoholics, opiate dependence subjects, methadone maintained subjects and mixed alcohol-opiate antecedents subjects compared with normal controls. Psychiatry Research, 119(3), 251260.CrossRefGoogle ScholarPubMed
Kornreich, C., Philippot, P., Foisy, M.L., Blairy, S., Raynaud, E., Dan, B., Hess, U., Noel, X., Pelc, I., & Verbanck, P. (2002). Impaired emotional facial expression recognition is associated with interpersonal problems in alcoholism. Alcohol and Alcoholism, 37(4), 394400.CrossRefGoogle ScholarPubMed
Lawrence, A.D., Goerendt, I.K., & Brooks, D.J. (2007). Impaired recognition of facial expressions of anger in Parkinson’s disease patients acutely withdrawn from dopamine replacement therapy. Neuropsychologia, 45(1), 6574.CrossRefGoogle ScholarPubMed
Leppanen, J.M., Milders, M., Bell, J.S., Terriere, E., & Hietanen, J.K. (2004). Depression biases the recognition of emotionally neutral faces. Psychiatry Research, 128(2), 123133.CrossRefGoogle ScholarPubMed
Masliah, E., DeTeresa, R.M., Mallory, M.E., & Hansen, L.A. (2000). Changes in pathological findings at autopsy in AIDS cases for the last 15 years. Aids, 14(1), 6974.CrossRefGoogle ScholarPubMed
Melrose, R.J., Tinaz, S., Castelo, J.M., Courtney, M.G., & Stern, C.E. (2008). Compromised fronto-striatal functioning in HIV: An fMRI investigation of semantic event sequencing. Behavioural Brain Research, 188(2), 337347.CrossRefGoogle ScholarPubMed
Morris, J.S., Friston, K.J., Buchel, C., Frith, C.D., Young, A.W., Calder, A.J., & Dolan, R.J. (1998). A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain, 121(Pt. 1), 4757.CrossRefGoogle ScholarPubMed
Murphy, F.C., Nimmo-Smith, I., & Lawrence, A.D. (2003). Functional neuroanatomy of emotions: A meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3(3), 207233.CrossRefGoogle ScholarPubMed
Pan, Y.J., Chen, S.H., Chen, W.J., & Liu, S.K. (2009). Affect recognition as an independent social function determinant in schizophrenia. Comprehensive Psychiatry, 50(5), 443452.CrossRefGoogle ScholarPubMed
Paul, R.H., Brickman, A.M., Navia, B., Hinkin, C., Malloy, P.F., Jefferson, A.L., Cohen, R.A., Tate, D.F., & Flanigan, T.P. (2005). Apathy is associated with volume of the nucleus accumbens in patients infected with HIV. Journal of Neuropsychiatry and Clinical Neurosciences, 17(2), 167171.CrossRefGoogle ScholarPubMed
Pfefferbaum, A., Rosenbloom, M.J., Adalsteinsson, E., & Sullivan, E.V. (2007). Diffusion tensor imaging with quantitative fibre tracking in HIV infection and alcoholism comorbidity: Synergistic white matter damage. Brain, 130(Pt. 1), 4864.CrossRefGoogle ScholarPubMed
Phan, K.L., Wager, T., Taylor, S.F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. Neuroimage, 16(2), 331348.CrossRefGoogle ScholarPubMed
Posamentier, M.T., & Abdi, H. (2003). Processing faces and facial expressions. Neuropsychology Review, 13(3), 113143.CrossRefGoogle ScholarPubMed
Radloff, L.S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1(3), 385401.CrossRefGoogle Scholar
Rapcsak, S.Z., Galper, S.R., Comer, J.F., Reminger, S.L., Nielsen, L., Kaszniak, A.W., Verfaellie, M., Laguna, J.F., Labiner, D.M., & Cohen, R.A. (2000). Fear recognition deficits after focal brain damage: A cautionary note. Neurology, 54(3), 575581.CrossRefGoogle ScholarPubMed
Rempel-Clower, N.L. (2007). Role of orbitofrontal cortex connections in emotion. Annals of the New York Academy of Sciences, 1121, 7286.CrossRefGoogle ScholarPubMed
Rubinow, D.R., & Post, R.M. (1992). Impaired recognition of affect in facial expression in depressed patients. Biological Psychiatry, 31(9), 947953.CrossRefGoogle ScholarPubMed
Shimokawa, A., Yatomi, N., Anamizu, S., Torii, S., Isono, H., Sugai, Y., & Kohno, M. (2001). Influence of deteriorating ability of emotional comprehension on interpersonal behavior in Alzheimer-type dementia. Brain and Cognition, 47(3), 423433.CrossRefGoogle ScholarPubMed
Simon, E.W., Rosen, M., Grossman, E., & Pratowski, E. (1995). The relationships among facial emotion recognition, social skills, and quality of life. Research in Developmental Disabilities, 16(5), 383391.CrossRefGoogle ScholarPubMed
Sprengelmeyer, R., Rausch, M., Eysel, U.T., & Przuntek, H. (1998). Neural structures associated with recognition of facial expressions of basic emotions. Proceedings. Biological Sciences, 265(1409), 19271931.CrossRefGoogle ScholarPubMed
Sprengelmeyer, R., Young, A.W., Calder, A.J., Karnat, A., Lange, H., Homberg, V., Perrett, D.I., & Rowland, D. (1996). Loss of disgust: Perception of faces and emotions in Huntington’s disease. Brain, 119(Pt. 5), 16471665.CrossRefGoogle ScholarPubMed
Sprengelmeyer, R., Young, A.W., Pundt, I., Sprengelmeyer, A., Calder, A.J., Berrios, G., Winkel, R., Vollmoeller, W., Kuhn, W., Sartory, G., & Przuntek, H. (1997). Disgust implicated in obsessive-compulsive disorder. Proceedings. Biological Sciences, 264(1389), 17671773.CrossRefGoogle ScholarPubMed
Stout, J.C., Ellis, R.J., Jernigan, T.L., Archibald, S.L., Abramson, I., Wolfson, T., McCutchan, J.A., Wallace, M.R., Atkinson, J.H., & Grant, I. (1998). Progressive cerebral volume loss in human immunodeficiency virus infection: A longitudinal volumetric magnetic resonance imaging study. HIV Neurobehavioral Research Center Group. Archives of Neurology, 55(2), 161168.CrossRefGoogle ScholarPubMed
Suzuki, A., Hoshino, T., Shigemasu, K., & Kawamura, M. (2006). Disgust-specific impairment of facial expression recognition in Parkinson’s disease. Brain, 129(Pt. 3), 707717.CrossRefGoogle ScholarPubMed
Tottenham, N., Tanaka, J.W., Leon, A.C., McCarry, T., Nurse, M., Hare, T.A., Marcus, D.J., Westerlund, A., Casey, B.J., & Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168(3), 242249.CrossRefGoogle ScholarPubMed
Tozzi, V., Balestra, P., Lorenzini, P., Bellagamba, R., Galgani, S., Corpolongo, A., Vlassi, C., Larussa, D., Zaccarelli, M., Noto, P., Visco-Comandini, U., Giulianelli, M., Ippolito, G., Antinori, A., & Narciso, P. (2005). Prevalence and risk factors for human immunodeficiency virus-associated neurocognitive impairment, 1996 to 2002: Results from an urban observational cohort. Journal of Neurovirology, 11(3), 265273.CrossRefGoogle ScholarPubMed
Valcour, V., Yee, P., Williams, A.E., Shiramizu, B., Watters, M., Selnes, O., Paul, R., Shikuma, C., & Sacktor, N. (2006). Lowest ever CD4 lymphocyte count (CD4 nadir) as a predictor of current cognitive and neurological status in human immunodeficiency virus type 1 infection—The Hawaii Aging with HIV Cohort. Journal of Neurovirology, 12(5), 387391.CrossRefGoogle ScholarPubMed
Wickline, V.B., Bailey, W., & Nowicki, S. (2009). Cultural in-group advantage: Emotion recognition in African American and European American faces and voices. Journal of Genetic Psychology, 170(1), 529.CrossRefGoogle ScholarPubMed
Wiley, C.A., Achim, C.L., Christopherson, C., Kidane, Y., Kwok, S., Masliah, E., Mellors, J., Radhakrishnan, L., Wang, G., & Soontornniyomkij, V. (1999). HIV mediates a productive infection of the brain. Aids, 13(15), 20552059.CrossRefGoogle ScholarPubMed