Decreased prefrontal cortical sensitivity to monetary reward is associated with impaired motivation and self-control in cocaine addiction

Rita Goldstein

Nelly Alia-Klein

Dardo Tomasi

Lei Zhang

Linda Chang+4 authors

^{Brookhaven National Laboratory, Upton, NY, 11973-5000}

^{SUNY at Stony Brook, Stony Brook, NY 11794-4400}

^{John A. Burns School of Medicine, University of Hawaii, Honolulu, HI 96813}

^{National Institute on Drug Abuse, Bethesda, MD 20892}

* Correspondence and Requests for materials should be addressed to: Rita Z. Goldstein, Brookhaven National Laboratory, P. O. Box 5000, Upton, NY, 11973-5000; tel. (631) 344-2657; fax (631) 344-5260; vog.lnb@nietsdlogr

Abstract

Objective

To examine the brain’s sensitivity to monetary rewards of different magnitudes in cocaine abusers and to study its association with motivation and self-control.

Method

Sixteen cocaine abusers and 13 matched healthy comparison subjects performed a forced-choice task under three monetary value conditions while brain activation was measured with functional magnetic resonance imaging. Objective measures of state motivation were assessed by reaction time and accuracy, and subjective measures were assessed by self-reports of task engagement. Measures of trait motivation and self-control were assessed with the Multidimensional Personality Questionnaire.

Results

The cocaine abusers demonstrated an overall reduced regional brain responsivity to differences between the monetary value conditions. Also, in comparison subjects but not in cocaine abusers reward-induced improvements in performance were associated with self-reports of task engagement, and money-induced activations in the lateral prefrontal cortex were associated with activations in the orbitofrontal cortex. For cocaine subjects, prefrontal cortex sensitivity to money was instead associated with motivation and self-control.

Conclusions

These findings suggest that in cocaine addiction (1) activation of the corticolimbic reward circuit to gradations of money is altered; (2) lack of a correlation between objective and subjective measures of state motivation may be indicative of disrupted perception of motivational drive, which could contribute to impairments in self-control; and (3) the lateral prefrontal cortex modulates trait motivation and deficits in self-control, and a possible underlying mechanism may encompass a breakdown in prefrontal-orbitofrontal cortical communication.

Abstract

Footnotes

Previous presentation. Presented in part as posters at the Annual Meetings of the Cognitive Neuroscience Society (New York, April 2005) and the American College on Neuropsychopharmacology (Hawaii, December 2005).

Footnotes

References

1. Goldstein RZ, Volkow NDDrug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry. 2002:1642–52.[Google Scholar]
2. Rollnick S, Heather N, Bell ANegotiating behaviour change in medical settings: the development of brief Motivational Interviewing. Journal of Mental Health. 1992;1:25–37.[PubMed][Google Scholar]
3. Garavan H, Pankiewicz J, Bloom A, Cho JK, Sperry L, Ross TJ, Salmeron BJ, Risinger R, Kelley D, Stein EACue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Am J Psychiatry. 2000;157(11):1789–98.[PubMed][Google Scholar]
4. Volkow ND, Wang GJ, Ma Y, Fowler JS, Wong C, Ding YS, Hitzemann R, Swanson JM, Kalivas PActivation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: relevance to addiction. J Neurosci. 2005;25(15):3932–9.[Google Scholar]
5. Kalivas PW, Volkow NDThe neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry. 2005;162(8):1403–13.[PubMed][Google Scholar]
6. Hikosaka K, Watanabe MDelay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. Cereb Cortex. 2000;10(3):263–71.[PubMed][Google Scholar]
7. Ochsner KN, Knierim K, Ludlow DH, Hanelin J, Ramachandran T, Glover G, Mackey SCReflecting upon feelings: an fMRI study of neural systems supporting the attribution of emotion to self and other. J Cogn Neurosci. 2004;16(10):1746–72.[PubMed][Google Scholar]
8. Hornak J, O’Doherty J, Bramham J, Rolls ET, Morris RG, Bullock PR, Polkey CEReward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J Cogn Neurosci. 2004;16(3):463–78.[PubMed][Google Scholar]
9. Gollub RL, Breiter HC, Kantor H, Kennedy D, Gastfriend D, Mathew RT, Makris N, Guimaraes A, Riorden J, Campbell T, Foley M, Hyman SE, Rosen B, Weisskoff RCocaine decreases cortical cerebral blood flow but does not obscure regional activation in functional magnetic resonance imaging in human subjects. J Cereb Blood Flow Metab. 1998;18(7):724–34.[PubMed][Google Scholar]
10. Volkow N, Ding Y, Fowler J, Wang G, Logan J, Gatley J, Dewey S, Ashby C, Liebermann J, Hitzemann R, Wolf AIs methylphenidate like cocaine? Studies on their pharmacokinetics and distribution in the human brain. Archives of General Psychiatry. 1995:456–463.[PubMed][Google Scholar]
11. Thut G, Schultz W, Roelcke U, Nienhusmeier M, Missimer J, Maguire RP, Leenders KLActivation of the human brain by monetary reward. Neuroreport. 1997;8(5):1225–8.[PubMed][Google Scholar]
12. Tellegen A, Waller NG. Exploring personality through test construction: development of the multidimensional personality questionnaire. In: Briggs SR, Cheek JM, editors. Personality measures: development and evaluation. Vol. 1. Greenwich: JAI Press; 1997. [PubMed]
13. Caparelli EC, Tomasi D, Arnold S, Chang L, Ernst Tk-Space based summary motion detection for functional magnetic resonance imaging. Neuroimage. 2003;20(2):1411–8.[PubMed][Google Scholar]
14. Lee JH, Garwood M, Menon R, Adriany G, Andersen P, Truwit CL, Ugurbil KHigh contrast and fast three-dimensional magnetic resonance imaging at high fields. Magn Reson Med. 1995;34(3):308–12.[PubMed][Google Scholar]
15. Ashburner J, Neelin P, Collins DL, Evans A, Friston KIncorporating prior knowledge into image registration. Neuroimage. 1997;6(4):344–52.[PubMed][Google Scholar]
16. Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSStatistical parametric maps in functional imaging: a general approach. Human Brain Mapping. 1995;2:189–210.[PubMed][Google Scholar]
17. Tomasi D, Ernst T, Caparelli EC, Chang LPractice-induced changes of brain function during visual attention: a parametric fMRI study at 4 Tesla. Neuroimage. 2004;23(4):1414–21.[PubMed][Google Scholar]
18. Talairach J, Tournoux P Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme Medical Publishers, Inc.; 1988. [PubMed][Google Scholar]
19. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans ACA unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping. 1996;4(1):58–73.[PubMed][Google Scholar]
20. Elliott R, Newman JL, Longe OA, Deakin JFDifferential response patterns in the striatum and orbitofrontal cortex to financial reward in humans: a parametric functional magnetic resonance imaging study. J Neurosci. 2003;23(1):303–7.[Google Scholar]
21. Tremblay L, Schultz WRelative reward preference in primate orbitofrontal cortex. Nature. 1999;398(6729):704–8.[PubMed][Google Scholar]
22. Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal PFunctional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron. 2001;30(2):619–39.[PubMed][Google Scholar]
23. Kringelbach ML, O’Doherty J, Rolls ET, Andrews CActivation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cereb Cortex. 2003;13(10):1064–71.[PubMed][Google Scholar]
24. Knutson B, Westdorp A, Kaiser E, Hommer DFMRI visualization of brain activity during a monetary incentive delay task. Neuroimage. 2000;12(1):20–7.[PubMed][Google Scholar]
25. O’Doherty J, Kringelbach ML, Rolls ET, Hornak J, Andrews CAbstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci. 2001;4(1):95–102.[PubMed][Google Scholar]
26. Watanabe MThe appropriateness of behavioral responses coded in post-trial activity of primate prefrontal units. Neurosci Lett. 1989;101(1):113–7.[PubMed][Google Scholar]
27. Tobler PN, Fiorillo CD, Schultz WAdaptive coding of reward value by dopamine neurons. Science. 2005;307(5715):1642–5.[PubMed][Google Scholar]
28. Bjork JM, Knutson B, Fong GW, Caggiano DM, Bennett SM, Hommer DWIncentive-elicited brain activation in adolescents: similarities and differences from young adults. J Neurosci. 2004;24(8):1793–802.[Google Scholar]
29. Goerendt IK, Lawrence AD, Brooks DJReward processing in health and Parkinson’s disease: neural organization and reorganization. Cereb Cortex. 2004;14(1):73–80.[PubMed][Google Scholar]
30. Hester R, Garavan HExecutive dysfunction in cocaine addiction: evidence for discordant frontal, cingulate, and cerebellar activity. J Neurosci. 2004;24(49):11017–22.[Google Scholar]
31. Bechara A, Tranel D, Damasio HCharacterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain. 2000;123 ( Pt 11):2189–202.[PubMed][Google Scholar]
32. Camille N, Coricelli G, Sallet J, Pradat-Diehl P, Duhamel JR, Sirigu AThe involvement of the orbitofrontal cortex in the experience of regret. Science. 2004;304(5674):1167–70.[PubMed][Google Scholar]
33. Volkow ND, Fowler JSAddiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex. 2000;10(3):318–25.[PubMed][Google Scholar]
34. Goldstein RZ, Volkow ND, Chang L, Wang GJ, Fowler JS, Depue RA, Gur RCThe orbitofrontal cortex in methamphetamine addiction: involvement in fear. Neuroreport. 2002;13(17):2253–7.[Google Scholar]
35. Goldstein RZ, Alia-Klein N, Leskovjan AC, Fowler JS, Wang GJ, Gur RC, Hitzemann R, Volkow NDAnger and depression in cocaine addiction: association with the orbitofrontal cortex. Psychiatry Research: Neuroimaging. in press. [[PubMed]
36. Goldstein RZ, Volkow ND, Wang GJ, Fowler JS, Rajaram SAddiction changes orbitofrontal gyrus function: involvement in response inhibition. Neuroreport. 2001;12(11):2595–9.[Google Scholar]
37. Lim KO, Choi SJ, Pomara N, Wolkin A, Rotrosen JPReduced frontal white matter integrity in cocaine dependence: a controlled diffusion tensor imaging study. Biol Psychiatry. 2002;51(11):890–5.[PubMed][Google Scholar]
38. Moeller FG, Hasan KM, Steinberg JL, Kramer LA, Dougherty DM, Santos RM, Valdes I, Swann AC, Barratt ES, Narayana PAReduced Anterior Corpus Callosum White Matter Integrity is Related to Increased Impulsivity and Reduced Discriminability in Cocaine-Dependent Subjects: Diffusion Tensor Imaging. Neuropsychopharmacology. 2005;30(3):610–7.[PubMed][Google Scholar]
39. Stein EA, Pankiewicz J, Harsch HH, Cho JK, Fuller SA, Hoffmann RG, Hawkins M, Rao SM, Bandettini PA, Bloom ASNicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiatry. 1998;155(8):1009–15.[PubMed][Google Scholar]
40. Volkow ND, Fowler JS, Wolf AP, Hitzemann R, Dewey S, Bendriem B, Alpert R, Hoff AChanges in brain glucose metabolism in cocaine dependence and withdrawal. Am J Psychiatry. 1991;148(5):621–6.[PubMed][Google Scholar]
41. McCambridge J, Strang JDeterioration over time in effect of Motivational Interviewing in reducing drug consumption and related risk among young people. Addiction. 2005;100(4):470–8.[PubMed][Google Scholar]