Abstract
Rationale
Current neurobiological models of addiction posit that drug seeking is much more likely to occur during emotionally charged states (such as craving), as deficits in inhibitory control become more pronounced during heightened motivational states.
Objective
The purpose of this study was to examine the effect of cue-induced craving states on attention and inhibitory control within addicted individuals.
Methods
We tested the performance of 39 opiate-dependent individuals on cognitive measures of attention (Digit Span, Digit Symbol, and Telephone Search) and inhibitory control (Counting Stroop and Go-No-Go) both before and after exposure to an autobiographical craving script. A non-drug using healthy control group (n = 19) performed the same tasks before and after listening to a relaxation tape.
Results
Following craving induction, opiate-dependent individuals demonstrated improved performance on tests of processing speed and attentional span (consistent with the practice effect observed in controls) and increased their response errors on the Stroop task (in contrast to controls), while selective attention was unaffected. Individual differences in compulsivity mediated the association between craving and Stroop performance, such that low-compulsive (but not high-compulsive) individuals committed more response errors after craving induction.
Conclusions
These findings challenge the notion of cue-induced craving as a primary trigger of disrupted cognition and drug-seeking behavior in addicted individuals, and raise the need to explore individual differences in compulsivity when addressing the links between craving and loss of control within research and clinical settings.
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References
Alfonso JP, Caracuel A, Delgado-Pastor LC, Verdejo-Garcia A (2011) Combined goal management training and mindfulness meditation improve executive functions and decision-making performance in abstinent polysubstance abusers. Drug Alcohol Depend. doi:10.1016/j.drugalcdep.2010.12.025
Beatty WW, Borrell GK (2000) Forms of knowledge, cognitive impairment and drug abuse: a demonstration. Prog Neuropsychopharmacol Biol Psychiatry 24:17–22
Beck AT, Steer RA (1993) Manual for Beck Anxiety Inventory. Psychological Corporation, San Antonio
Beck AT, Steer RA, Brown GK (1996) The Beck Depression Inventory–second edition. The Psychological Corporation, San Antonio
Beglinger LJ, Gaydos B, Tangphao-Daniels O, Duff K, Kareken DA, Crawford J, Fastenau PS, Siemers ER (2005) Practice effects and the use of alternate forms in serial neuropsychological testing. Arch Clin Neuropsychol 20:517–529
Belin D, Mar AC, Dalley JW, Robbins TW, Everitt BJ (2008) High impulsivity predicts the switch to compulsive cocaine-taking. Science 320:1352–1355
Brewer JA, Worhunsky PD, Carroll KM, Rounsaville BJ, Potenza MN (2008) Pretreatment brain activation during stroop task is associated with outcomes in cocaine-dependent patients. Biol Psychiatry 64:998–1004
Bush G, Whalen PJ, Shin LM, Rauch SL (2006) The counting Stroop: a cognitive interference task. Nat Protoc 1:230–233
Carter BL, Tiffany ST (1999) Meta-analysis of cue-reactivity in addiction research. Addiction 94:327–340
Chambers CD, Garavan H, Bellgrove MA (2009) Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neurosci Biobehav Rev 33:631–646
Ciccocioppo R, Martin-Fardon R, Weiss F (2004) Stimuli associated with a single cocaine experience elicit long-lasting cocaine-seeking. Nat Neurosci 7:495–496
Constantinou N, Morgan CJ, Battistella S, O’Ryan D, Davis P, Curran HV (2010) Attentional bias, inhibitory control and acute stress in current and former opiate addicts. Drug Alcohol Depend 109:220–225
Daglish MR, Weinstein A, Malizia AL, Wilson S, Melichar JK, Lingford-Hughes A, Myles JS, Grasby P, Nutt DJ (2003) Functional connectivity analysis of the neural circuits of opiate craving: “more” rather than “different”? NeuroImage 20:1964–1970
Drummond DC, Litten RZ, Lowman C, Hunt WA (2000) Craving research: future directions. Addiction 95:247–255
Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489
First MB, Spitzer RL, Gibbon M, Williams JBW (1996) Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). American Psychiatric Press Inc, Washington DC
Franken IH (2003) Drug craving and addiction: integrating psychological and neuropsychopharmacological approaches. Prog Neuropsychopharmacol Biol Psychiatry 27:563–579
Franken IH, Hendriksa VM, van den Brink W (2002) Initial validation of two opiate craving questionnaires the obsessive compulsive drug use scale and the desires for drug questionnaire. Addict Behav 27:675–685
Goldstein RZ, Woicik PA, Lukasik T, Maloney T, Volkow ND (2007) Drug fluency: a potential marker for cocaine use disorders. Drug Alcohol Depend 89:97–101
Gossop M, Darke S, Griffiths P, Hando J, Powis B, Hall W, Strang J (1995) The Severity of Dependence Scale (SDS): psychometric properties of the SDS in English and Australian samples of heroin, cocaine and amphetamine users. Addiction 90:607–614
Gossop M, Best D, Marsden J, Strang J (1997) Test–retest reliability of the Severity of Dependence Scale. Addiction 92:353
Hartwell KJ, Johnson KA, Li X, Myrick H, Lematty T, George MS, Brady KT (2011) Neural correlates of craving and resisting craving for tobacco in nicotine dependent smokers. Addict Biol 16:654–666
Hester R, Garavan H (2009) Neural mechanisms underlying drug-related cue distraction in active cocaine users. Pharmacol Biochem Behav 93:270–277
Hogarth L (2011) The role of impulsivity in the aetiology of drug dependence: reward sensitivity versus automaticity. Psychopharmacology (Berl). doi:10.1007/s00213-011-2172-0
Lubman DI, Yücel M, Pantelis C (2004) Addiction, a condition of compulsive behaviour? Neuroimaging and neuropsychological evidence of inhibitory dysregulation. Addiction 99:1491–1502
Lubman DI, Yücel M, Kettle JW, Scaffidi A, Mackencie T, Simmons JG, Allen NB (2009) Responsiveness to drug cues and natural rewards in opiate addiction: associations with later heroin use. Arch Gen Psychiatry 66:205–212
Mintzer MZ, Stitzer ML (2002) Cognitive impairment in methadone maintenance patients. Drug Alcohol Depend 67:41–51
Robertson IH, Ward T, Ridgeway V, Nimmo-Smith I (1994) The Test of Everyday Attention. Thames Valley Test Company, Bury
Robertson IH, Ward T, Ridgeway V, Nimmo-Smith I (1996) The structure of normal human attention: The Test of Everyday Attention. J Int Neuropsychol Soc 2:525–534
Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247–291
Seignourel PJ, Green C, Schmitz JM (2008) Factor structure and diagnostic efficiency of the BDI-II in treatment-seeking substance users. Drug Alcohol Depend 93:271–278
Sinha R, Talih M, Malison R, Cooney N, Anderson GM, Kreek MJ (2003) Hypothalamic-pituitary-adrenal axis and sympatho-adreno-medullary responses during stress-induced and drug cue-induced cocaine craving states. Psychopharmacology (Berl) 170:62–72
Sofuoglu M (2010) Cognitive enhancement as a pharmacotherapy target for stimulant addiction. Addiction 105:38–48
Takagi M, Lubman DI, Cotton S, Fornito A, Baliz Y, Tucker A, Yucel M (2010) Executive control among adolescent inhalant and cannabis users. Drug Alcohol Rev. doi:10.1111/j.1465-3362.2010.00256.x
Tiffany ST (1990) A cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. Psychol Rev 97:147–168
Verdejo A, Toribio I, Orozco C, Puente KL, Perez-Garcia M (2005) Neuropsychological functioning in methadone maintenance patients versus abstinent heroin abusers. Drug Alcohol Depend 78:283–288
Verdejo-García A, Bechara A (2009) A somatic marker theory of addiction. Neuropharmacology 56:48–62
Volkow ND, Fowler JS, Wang GJ, Telang F, Logan J, Jayne M, Ma Y, Pradhan K, Wong C, Swanson JM (2010) Cognitive control of drug craving inhibits brain reward regions in cocaine abusers. NeuroImage 49:2536–2543
Wechsler D (1997) WAIS-III administration and scoring manual. The Psychological Corporation, San Antonio
Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence. The Psychological Corporation, San Antonio
Weiss F (2005) Neurobiology of craving, conditioned reward and relapse. Curr Opin Pharmacol 5:9–19
Wilson SJ, Sayette MA, Fiez JA (2004) Prefrontal responses to drug cues: a neurocognitive analysis. Nat Neurosci 7:211–214
Yücel M, Lubman DI, Harrison BJ, Fornito A, Allen NB, Wellard RM, Roffel K, Clarke K, Wood SJ, Forman SD, Pantelis C (2007) A combined spectroscopic and functional MRI investigation of the dorsal anterior cingulate region in opiate addiction. Mol Psychiatry 12:691–702
Acknowledgments
Dr. Yücel is supported by a National Health and Medical Research Council Clinical Career Development Award (grant 509345). Dr. Verdejo-García is supported by a José Castillejo Fellowship from the Spanish Ministry of Education and Science (JC2010-0195). Dr. Vilar-López is supported by a José Castillejo Fellowship from the Spanish Ministry of Education and Science (JC2010-0193).
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Table 1 supplementary material
Demographic and clinical characteristics of opiate-dependent participants classified as high vs. low compulsive by median split on the YBOCSUD scale (DOC 30 kb)
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Verdejo-García, A., Lubman, D.I., Schwerk, A. et al. Effect of craving induction on inhibitory control in opiate dependence. Psychopharmacology 219, 519–526 (2012). https://doi.org/10.1007/s00213-011-2512-0
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DOI: https://doi.org/10.1007/s00213-011-2512-0