fMRI brain activation during a delay discounting task in HIV-positive adults with and without cocaine dependence

Cocaine use is associated with poorer HIV clinical outcomes and may contribute to neurobiological impairments associated with impulsive decision making. This study examined the effect of cocaine dependence on brain activation during a delay discounting task involving choices between smaller immediate rewards and larger delayed ones. Participants were 39 HIV-positive adults on antiretroviral therapy who had current cocaine dependence ("active," n=15), past cocaine dependence ("recovered," n=13), or no lifetime substance dependence ("naïve," n=11). Based on responses on a traditional delay discounting task, three types of choices were individualized for presentation during functional magnetic resonance imaging: hard (similarly valued), easy (disparately valued), and no (single option). Active participants had significantly smaller increases in activation than naïve participants during hard versus easy choices bilaterally in the precentral gyrus and anterior cingulate cortex and in the right frontal pole (including dorsolateral, ventrolateral, and orbitofrontal cortex). During hard and easy choices relative to no choices, active participants had smaller increases in activation compared to naïve participants in frontoparietal cortical regions. These deficits in the executive network during delay discounting choices may contribute to impulsive decision making among HIV-positive cocaine users, with implications for risk behaviors associated with disease transmission and progression.

[1]  B. Brew,et al.  Neuropsychological Functioning and Antiretroviral Treatment in HIV/AIDS: A Review , 2009, Neuropsychology Review.

[2]  Michael J. Taylor,et al.  The HNRC 500-Neuropsychology of Hiv infection at different disease stages , 1995, Journal of the International Neuropsychological Society.

[3]  W. Bickel,et al.  Shortened time horizons and insensitivity to future consequences in heroin addicts. , 1998, Addiction.

[4]  W. Bickel,et al.  Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. , 1999 .

[5]  Linda Chang,et al.  Declined neural efficiency in cognitively stable human immunodeficiency virus patients , 2009, Annals of neurology.

[6]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[7]  D. Metzger,et al.  The Fifth Edition of the Addiction Severity Index. , 1992, Journal of substance abuse treatment.

[8]  P. Cinque,et al.  Spatial working memory in asymptomatic HIV-infected subjects. , 1999, The Journal of neuropsychiatry and clinical neurosciences.

[9]  J. E. Mazur,et al.  Tests of transitivity in choices between fixed and variable reinforcer delays. , 1987, Journal of the experimental analysis of behavior.

[10]  A. Toga,et al.  Thinning of the cerebral cortex visualized in HIV/AIDS reflects CD4+ T lymphocyte decline , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Seidenberg,et al.  Verbal working memory in HIV-seropositive drug users , 2000, Journal of the International Neuropsychological Society.

[12]  C. Sherbourne,et al.  Psychosocial mediators of antiretroviral nonadherence in HIV-positive adults with substance use and mental health problems. , 2004, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[13]  T. Hergueta,et al.  The mini international neuropsychiatric interview , 1998, European Psychiatry.

[14]  J. Jovicich,et al.  Abnormal brain activation on functional MRI in cognitively asymptomatic HIV patients , 2002, Neurology.

[15]  Stacey B. Daughters,et al.  Differences in impulsivity and sexual risk behavior among inner-city crack/cocaine users and heroin users. , 2005, Drug and alcohol dependence.

[16]  Gal Meiri,et al.  Cortical activation during delay discounting in abstinent methamphetamine dependent individuals , 2008, Psychopharmacology.

[17]  P. C. Fletcher,et al.  Abnormal frontal activations related to decision-making in current and former amphetamine and opiate dependent individuals , 2005, Psychopharmacology.

[18]  Matthew W. Johnson,et al.  Delay discounting in currently using and currently abstinent cocaine-dependent outpatients and non-drug-using matched controls. , 2006, Addictive behaviors.

[19]  Mardge H. Cohen,et al.  Crack cocaine, disease progression, and mortality in a multicenter cohort of HIV-1 positive women , 2008, AIDS.

[20]  Laurie C. Zephyrin,et al.  Health-related quality of life in HIV-infected patients: the role of substance use. , 2008, AIDS patient care and STDs.

[21]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[22]  M. Paulus,et al.  Location, location: using functional magnetic resonance imaging to pinpoint brain differences relevant to stimulant use. , 2007, Addiction.

[23]  E. Masliah,et al.  Neurobiology of HIV , 2008, International review of psychiatry.

[24]  K. Brady,et al.  Impulsivity and rapid discounting of delayed hypothetical rewards in cocaine-dependent individuals. , 2003, Experimental and clinical psychopharmacology.

[25]  S. Mitchell,et al.  Neuropsychological function and delay discounting in methamphetamine-dependent individuals , 2006, Psychopharmacology.

[26]  C. M. Bradshaw,et al.  Quantification of Steady-State Operant Behavior , 1982 .

[27]  R. Grant,et al.  Impact of active drug use on antiretroviral therapy adherence and viral suppression in HIV-infected drug users. , 2002 .

[28]  A. Bechara,et al.  Cognitive impulsivity and HIV serostatus in substance dependent males , 2004, Journal of the International Neuropsychological Society.

[29]  Stacey B. Daughters,et al.  Risk-taking propensity and risky sexual behavior of individuals in residential substance use treatment. , 2004, Addictive behaviors.

[30]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[31]  D. D. Des Jarlais,et al.  Initiation of regular marijuana use among a cohort of women infected with or at risk for HIV in the Women's Interagency HIV Study (WIHS). , 2004, AIDS patient care and STDs.

[32]  Daniel Tranel,et al.  Executive control deficits in substance-dependent individuals: A comparison of alcohol, cocaine, and methamphetamine and of men and women , 2009, Journal of clinical and experimental neuropsychology.

[33]  M. Gladis,et al.  Retention in psychosocial treatment of cocaine dependence: predictors and impact on outcome. , 2002, The American journal on addictions.

[34]  H Rachlin,et al.  Commitment, choice and self-control. , 1972, Journal of the experimental analysis of behavior.

[35]  A. Verdejo‐Garcia,et al.  Cognitive impulsivity in cocaine and heroin polysubstance abusers. , 2007, Addictive behaviors.

[36]  M. Stein,et al.  Sexual risk behaviors among substance users: relationship to impulsivity. , 2006, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[37]  C. Sherbourne,et al.  Psychiatric disorders and drug use among human immunodeficiency virus-infected adults in the United States. , 2001, Archives of general psychiatry.

[38]  Saori C. Tanaka,et al.  Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops , 2004, Nature Neuroscience.

[39]  George Ainslie,et al.  Frontoparietal cortical activity of methamphetamine‐dependent and comparison subjects performing a delay discounting task , 2007, Human brain mapping.

[40]  Walter Schneider,et al.  The cognitive control network: Integrated cortical regions with dissociable functions , 2007, NeuroImage.

[41]  I. Grant,et al.  Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons , 2004, Journal of the International Neuropsychological Society.

[42]  M. Webber,et al.  A prospective study of HIV disease progression in female and male drug users. , 1999, AIDS.

[43]  Mardge H. Cohen,et al.  Illicit drug use, depression and their association with highly active antiretroviral therapy in HIV-positive women. , 2007, Drug and alcohol dependence.

[44]  I. Grant,et al.  HIV-associated prospective memory impairment increases risk of dependence in everyday functioning. , 2008, Neuropsychology.

[45]  D. Hatsukami,et al.  Sex and menstrual cycle differences in the subjective effects from smoked cocaine in humans. , 1999, Experimental and clinical psychopharmacology.

[46]  Kris N Kirby,et al.  Heroin and cocaine abusers have higher discount rates for delayed rewards than alcoholics or non-drug-using controls. , 2004, Addiction.

[47]  A. J. Harzke,et al.  Binge Use of Crack Cocaine and Sexual Risk Behaviors Among African-American, HIV-Positive Users , 2009, AIDS and Behavior.

[48]  J. Bell,et al.  The Neuropathology of HIV/AIDS , 2008, International review of psychiatry.

[49]  A. Bechara,et al.  The influence of executive functions, sensation seeking, and HIV serostatus on the risky sexual practices of substance-dependent individuals , 2005, Journal of the International Neuropsychological Society.

[50]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

[51]  G. Ainslie Specious reward: a behavioral theory of impulsiveness and impulse control. , 1975, Psychological bulletin.

[52]  E. Costenbader,et al.  Stimulant use and sexual risk behaviors for HIV in rural North Carolina. , 2007, The Journal of rural health : official journal of the American Rural Health Association and the National Rural Health Care Association.

[53]  S. Lai,et al.  Crack-Cocaine Use Accelerates HIV Disease Progression in a Cohort of HIV-Positive Drug Users , 2009, Journal of acquired immune deficiency syndromes.

[54]  D. Tomasi,et al.  Adaptation of the attention network in human immunodeficiency virus brain injury , 2004, Annals of neurology.

[55]  Bruce J Brew,et al.  Evidence for a change in AIDS dementia complex in the era of highly active antiretroviral therapy and the possibility of new forms of AIDS dementia complex. , 2004, AIDS.

[56]  A. Levine,et al.  Risky decision making assessed with the gambling task in adults with HIV. , 2006, Neuropsychology.

[57]  E. Martin,et al.  Delayed recognition memory span in HIV-1 infection , 1995, Journal of the International Neuropsychological Society.

[58]  Chantal E. Stern,et al.  Compromised fronto-striatal functioning in HIV: An fMRI investigation of semantic event sequencing , 2008, Behavioural Brain Research.

[59]  T. Ernst,et al.  Neural correlates of attention and working memory deficits in HIV patients , 2001, Neurology.

[60]  K. Kieburtz,et al.  Cognitive performance and regional brain volume in human immunodeficiency virus type 1 infection. , 1996, Archives of neurology.

[61]  Mahendra Kumar,et al.  Human immunodeficiency virus type 1 RNA Levels in different regions of human brain: Quantification using real-time reverse transcriptase-polymerase chain reaction , 2011, Journal of NeuroVirology.

[62]  T. Lyons,et al.  Stimulant use and HIV risk behavior: the influence of peer support group participation. , 2006, AIDS education and prevention : official publication of the International Society for AIDS Education.

[63]  H. Myers,et al.  Drug Use and Medication Adherence among HIV-1 Infected Individuals , 2007, AIDS and Behavior.