Impaired neural response to negative prediction errors in cocaine addiction

Journal of Neuroscience

Volumn 35, Issue 5, 2015, Pages 1872-1879

  Parvaz, Muhammad A ^a   Konova, Anna B ^b   Proudfit, Greg H ^c   Dunning, Jonathan P ^d   Malaker, Pias ^a   Moeller, Scott J ^a   Maloney, Tom ^a   Alia Klein, Nelly ^a   Goldstein, Rita Z ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d NEVADA STATE COLLEGE   (United States)

Author keywords

Addiction; Cocaine; Event related potentials; Feedback negativity; Reward prediction error; Self medication

Indexed keywords

COCAINE;

ADULT; ARTICLE; CLINICAL ARTICLE; COCAINE DEPENDENCE; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; FEEDBACK RELATED NEGATIVITY; FEEDBACK SYSTEM; FEMALE; HUMAN; LEARNING; MALE; NERVE POTENTIAL; NERVE STIMULATION; PRIORITY JOURNAL; SCORING SYSTEM; TASK PERFORMANCE; TOPOGRAPHY; ADAPTIVE BEHAVIOR; CASE CONTROL STUDY; EVOKED RESPONSE; MIDDLE AGED; PATHOPHYSIOLOGY; REWARD;

ADULT; CASE-CONTROL STUDIES; COCAINE-RELATED DISORDERS; EVOKED POTENTIALS; FEEDBACK, PSYCHOLOGICAL; FEMALE; HUMANS; MALE; MIDDLE AGED; REWARD;

EID: 84922387951     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2777-14.2015     Document Type: Article

References (80)

1. Balodis IM, Kober H, Worhunsky PD, Stevens MC, Pearlson GD, Potenza MN (2012) Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling. Biol Psychiatry 71:749–757.CrossRef Medline
2. Beck AT, Steer RA, Ball R, Ranieri W (1996) Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. J Pers Assess 67: 588–597.CrossRef Medline
3. Carlson JM, Foti D, Mujica-Parodi LR, Harmon-Jones E, Hajcak G (2011) Ventral striatal and medial prefrontal BOLD activation is correlated with reward-related electrocortical activity: a combined ERP and fMRI study. Neuroimage 57:1608–1616.CrossRef Medline
4. Chiu PH, Lohrenz TM, Montague PR (2008) Smokers’ brains compute, but ignore, a fictive error signal in a sequential investment task. Nat Neurosci 11:514–520.CrossRef Medline
5. Ciccocioppo R, Sanna PP, Weiss F (2001) Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists. Proc Natl Acad Sci U S A 98:1976–1981.CrossRef Medline
6. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N (2012) Neuron-typespecific signals for reward and punishment in the ventral tegmental area. Nature 482:85–88.CrossRef Medline
7. Cools R, Robinson OJ, Sahakian B (2008) Acute tryptophan depletion in healthy volunteers enhances punishment prediction but does not affect reward prediction. Neuropsychopharmacology 33:2291–2299.CrossRef Medline
8. Daw ND, Kakade S, Dayan P (2002) Opponent interactions between serotonin and dopamine. Neural Netw 15:603–616.CrossRef Medline
9. Di Chiara G (1998) A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J Psychopharmacol 12:54–67.CrossRef Medline
10. Dunning JP, Parvaz MA, Hajcak G, Maloney T, Alia-Klein N, Woicik PA, Telang F, Wang GJ, Volkow ND, Goldstein RZ (2011) Motivated attention to cocaine and emotional cues in abstinent and current cocaine users—an ERP study. Eur J Neurosci 33:1716–1723.CrossRef Medline
11. Ersche KD, Roiser JP, Robbins TW, Sahakian BJ (2008) Chronic cocaine but not chronic amphetamine use is associated with perseverative responding in humans. Psychopharmacology (Berl) 197:421–431.CrossRef Medline
12. Euser AS, van Meel CS, Snelleman M, Franken IH (2011) Acute effects of alcohol on feedback processing and outcome evaluation during risky decision-making: an ERP study. Psychopharmacology (Berl) 217:111–125.CrossRef Medline
13. Euser AS, Greaves-Lord K, Crowley MJ, Evans BE, Huizink AC, Franken IH (2013) Blunted feedback processing during risky decision making in adolescents with a parental history of substance use disorders. Dev Psychopathol 25:1119–1136.CrossRef Medline
14. Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489.CrossRef Medline
15. Fein G, Chang M (2008) Smaller feedback ERN amplitudes during the BART are associated with a greater family history density of alcohol problems in treatment-naive alcoholics. Drug Alcohol Depend 92:141–148.CrossRef Medline
16. First MB, Gibbon M, Spitzer RL (1996) User’s guide for the structured clinical interview for Axis I DSM-IV Disorders—Research Version. New York: Biometrics Research.
17. Frank MJ, Claus ED (2006) Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychol Rev 113:300–326.CrossRef Medline
18. Franken IH, Van den Berg I, Van Strien JW (2010) Individual differences in alcohol drinking frequency are associated with electrophysiological responses to unexpected nonrewards. Alcohol Clin Exp Res 34:702–707.CrossRef Medline
19. Garavan H, Kaufman JN, Hester R (2008) Acute effects of cocaine on the neurobiology of cognitive control. Philos Trans R Soc Lond B Biol Sci 363:3267–3276.CrossRef Medline
20. George O, Mandyam CD, Wee S, Koob GF (2008) Extended access to cocaine self-administration produces long-lasting prefrontal cortexdependent working memory impairments. Neuropsychopharmacology 33:2474–2482.CrossRef Medline
21. Glimcher PW (2011) Understanding dopamine and reinforcement learning: the dopamine reward prediction error hypothesis. Proc Natl Acad Sci U S A 108 [Suppl 3]:15647–15654.CrossRef Medline
22. Goldstein RZ, Woicik PA, Maloney T, Tomasi D, Alia-Klein N, Shan J, Honorio J, Samaras D, Wang R, Telang F, Wang GJ, Volkow ND (2010) Oral methylphenidate normalizes cingulate activity in cocaine addiction during a salient cognitive task. Proc Natl Acad Sci U S A 107:16667–16672.CrossRef Medline
23. Gossop M, Griffiths P, Powis B, Strang J (1992) Severity of dependence and route of administration of heroin, cocaine and amphetamines. Br J Addict 87:1527–1536.CrossRef Medline
24. Gradin VB, Baldacchino A, Balfour D, Matthews K, Steele JD (2014) Abnormal brain activity during a reward and loss task in opiate-dependent patients receiving methadone maintenance therapy. Neuropsychopharmacology 39:885–894.CrossRef Medline
25. Hajcak G, Moser JS, Holroyd CB, Simons RF (2007) It’s worse than you thought: the feedback negativity and violations of reward prediction in gambling tasks. Psychophysiology 44:905–912.CrossRef Medline
26. Hart AS, Rutledge RB, Glimcher PW, Phillips PE (2014) Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term. J Neurosci 34:698–704.CrossRef Medline
27. Hauser TU, Iannaccone R, Stämpfli P, Drechsler R, Brandeis D, Walitza S, Brem S (2014) The feedback-related negativity (FRN) revisited: new insights into the localization, meaning and network organization. Neuroimage 84:159–168.CrossRef Medline
28. Hollerman JR, Schultz W (1998) Dopamine neurons report an error in the temporal prediction of reward during learning. Nat Neurosci 1:304–309.CrossRef Medline
29. Holroyd CB, Nieuwenhuis S, Yeung N, Cohen JD (2003) Errors in reward prediction are reflected in the event-related brain potential. Neuroreport 14:2481–2484.CrossRef Medline
30. Holroyd CB, Pakzad-Vaezi KL, Krigolson OE (2008) The feedback correctrelated positivity: sensitivity of the event-related brain potential to unexpected positive feedback. Psychophysiology 45:688–697.CrossRef Medline
31. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565–598.CrossRef Medline
32. Jones SR, Garris PA, Wightman RM (1995) Different effects of cocaine and nomifensine on dopamine uptake in the caudate-putamen and nucleus accumbens. J Pharmacol Exp Ther 274:396–403.Medline
33. Kampman KM, Volpicelli JR, McGinnis DE, Alterman AI, Weinrieb RM, D’Angelo L, Epperson LE (1998) Reliability and validity of the Cocaine Selective Severity Assessment. Addict Behav 23:449–461.CrossRef Medline
34. Khantzian EJ (1997) The self-medication hypothesis of substance use disorders: a reconsideration and recent applications. Harv Rev Psychiatry 4:231–244.CrossRef Medline
35. Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24:97–129.CrossRef Medline
36. Koob GF, Sanna PP, Bloom FE (1998) Neuroscience of addiction. Neuron 21:467–476.CrossRef Medline
37. Lawson RP, Seymour B, Loh E, Lutti A, Dolan RJ, Dayan P, Weiskopf N, Roiser JP (2014) The habenula encodes negative motivational value associated with primary punishment in humans. Proc Natl Acad Sci U S A 111:11858–11863.CrossRef Medline
38. Lesieur HR, Blume SB (1987) The South Oaks Gambling Screen (SOGS): a new instrument for the identification of pathological gamblers. Am J Psychiatry 144:1184–1188. Medline
39. Liu S, Heitz RP, Sampson AR, Zhang W, Bradberry CW (2008) Evidence of temporal cortical dysfunction in rhesus monkeys following chronic cocaine self-administration. Cereb Cortex 18:2109–2116.CrossRef Medline
40. Liu X, Powell DK, Wang H, Gold BT, Corbly CR, Joseph JE (2007) Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. J Neurosci 27:4587–4597.CrossRef Medline
41. Maia TV, Frank MJ (2011) From reinforcement learning models to psychiatric and neurological disorders. Nat Neurosci 14:154–162.CrossRef Medline
42. Martinez D, Greene K, Broft A, Kumar D, Liu F, Narendran R, Slifstein M, Van Heertum R, Kleber HD (2009) Lower level of endogenous dopamine in patients with cocaine dependence: findings from PET imaging of D(2)/D(3) receptors following acute dopamine depletion. Am J Psychiatry 166:1170–1177.CrossRef Medline
43. Matsumoto M, Hikosaka O (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111–1115.CrossRef Medline
44. Matuskey D, Bhagwagar Z, Planeta B, Pittman B, Gallezot JD, Chen J, Wanyiri J, Najafzadeh S, Ropchan J, Geha P, Huang Y, Potenza MN, Neumeister A, Carson RE, Malison RT (2014) Reductions in brain 5-HT receptor availability in primarily cocaine-dependent humans. Biol Psychiatry 76: 816–822.CrossRef Medline
45. McClure SM, Berns GS, Montague PR (2003) Temporal prediction errors in a passive learning task activate human striatum. Neuron 38:339–346.CrossRef Medline
46. McLellan AT, Kushner H, Metzger D, Peters R, Smith I, Grissom G, Pettinati H, ArgeriouM (1992) The Fifth Edition of the Addiction Severity Index. J Subst Abuse Treat 9:199–213.CrossRef Medline
47. Melis M, Spiga S, Diana M (2005) The dopamine hypothesis of drug addiction: hypodopaminergic state. Int Rev Neurobiol 63:101–154.CrossRef Medline
48. Mirenowicz J, Schultz W (1994) Importance of unpredictability for reward responses in primate dopamine neurons. J Neurophysiol 72:1024–1027.Medline
49. Moeller SJ, Maloney T, Parvaz MA, Alia-Klein N, Woicik PA, Telang F, Wang GJ, Volkow ND, Goldstein RZ (2010) Impaired insight in cocaine addiction: laboratory evidence and effects on cocaine-seeking behaviour. Brain 133:1484–1493.CrossRef Medline
50. Moeller SJ, Parvaz MA, Shumay E, Beebe-Wang N, Konova AB, Alia-Klein N, Volkow ND, Goldstein RZ (2013) Gene abstinence effects on drug cue reactivity in addiction: multimodal evidence. J Neurosci 33:10027–10036.CrossRef Medline
51. Montague PR, Hyman SE, Cohen JD (2004) Computational roles for dopamine in behavioural control. Nature 431:760–767.CrossRef Medline
52. Muñoz MÁ, Anllo-Vento L, del Carmen Fernández M, Montoya P, Vila J (2012) Modulation of the outcome-related negativity associated with nicotine abstinence. Exp Clin Psychopharmacol 20:151–160.CrossRef Medline
53. Nieuwenhuis S, Holroyd CB, Mol N, Coles MG (2004a) Reinforcementrelated brain potentials from medial frontal cortex: origins and functional significance. Neurosci Biobehav Rev 28:441–448.CrossRef Medline
54. Nieuwenhuis S, Yeung N, Holroyd CB, Schurger A, Cohen JD (2004b) Sensitivity of electrophysiological activity from medial frontal cortex to utilitarian and performance feedback. Cereb Cortex 14:741–747.CrossRef Medline
55. Nolte G, Hämäläinen MS (2001) Partial signal space projection for artefact removal in MEG measurements: a theoretical analysis. Phys Med Biol 46:2873–2887.CrossRef Medline
56. Oliveira FT, McDonald JJ, Goodman D (2007) Performance monitoring in the anterior cingulate is not all error related: expectancy deviation and the representation of action–outcome associations. J Cogn Neurosci 19: 1994–2004.CrossRef Medline
57. Park SQ, Kahnt T, Beck A, Cohen MX, Dolan RJ, Wrase J, Heinz A (2010) Prefrontal cortex fails to learn from reward prediction errors in alcohol dependence. J Neurosci 30:7749–7753.CrossRef Medline
58. Parvaz MA, Maloney T, Moeller SJ, Woicik PA, Alia-Klein N, Telang F, Wang GJ, Squires NK, Volkow ND, Goldstein RZ (2012) Sensitivity to monetary reward is most severely compromised in recently abstaining cocaine addicted individuals: a cross-sectional ERP study. Psychiatry Res 203:75–82.CrossRef Medline
59. Pfabigan DM, Alexopoulos J, Bauer H, Sailer U (2011) Manipulation of feedback expectancy and valence induces negative and positive reward prediction error signals manifest in event-related brain potentials. Psychophysiology 48:656–664.CrossRef Medline
60. Porter JN, Olsen AS, Gurnsey K, Dugan BP, Jedema HP, Bradberry CW (2011) Chronic cocaine self-administration in rhesus monkeys: impact on associative learning, cognitive control, and working memory. J Neurosci 31:4926–4934.CrossRef Medline
61. Reynolds JN, Hyland BI, Wickens JR (2001) A cellular mechanism of reward-related learning. Nature 413:67–70.CrossRef Medline
62. Rice ME, Cragg SJ (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7:583–584.CrossRef Medline
63. Rose EJ, Ross TJ, Salmeron BJ, Lee M, Shakleya DM, Huestis M, Stein EA (2012) Chronic exposure to nicotine is associated with reduced rewardrelated activity in the striatum but not the midbrain. Biol Psychiatry 71: 206–213.CrossRef Medline
64. Rose EJ, Salmeron BJ, Ross TJ, Waltz J, Schweitzer JB, McClure SM, Stein EA (2014) Temporal difference error prediction signal dysregulation in cocaine dependence. Neuropsychopharmacology 39:1732–1742.CrossRef Medline
65. Schoenbaum G, Saddoris MP, Ramus SJ, Shaham Y, Setlow B (2004) Cocaine-experienced rats exhibit learning deficits in a task sensitive to orbitofrontal cortex lesions. Eur J Neurosci 19:1997–2002.CrossRef Medline
66. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27. Medline
67. Schultz W (2011) Potential vulnerabilities of neuronal reward, risk, and decision mechanisms to addictive drugs. Neuron 69:603–617.CrossRef Medline
68. Schultz W, Romo R (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum. Exp Brain Res 91:363–384.Medline
69. Stern WC, Johnson A, Bronzino JD, Morgane PJ (1981) Neuropharmacology of the afferent projections from the lateral habenula and substantia nigra to the anterior raphe in the rat. Neuropharmacology 20:979–989.CrossRef Medline
70. Talmi D, Atkinson R, El-Deredy W (2013) The feedback-related negativity signals salience prediction errors, not reward prediction errors. J Neurosci 33:8264–8269.CrossRef Medline
71. Tanabe J, Reynolds J, Krmpotich T, Claus E, Thompson LL, Du YP, Banich MT (2013) Reduced neural tracking of prediction error in substancedependent individuals. Am J Psychiatry 170:1356–1363.CrossRef Medline
72. Tiffany ST, Singleton E, Haertzen CA, Henningfield JE (1993) The development of a cocaine craving questionnaire. Drug Alcohol Depend 34:19–28.CrossRef Medline
73. Tomasi D, Goldstein RZ, Telang F, Maloney T, Alia-Klein N, Caparelli EC, Volkow ND (2007) Widespread disruption in brain activation patterns to a working memory task during cocaine abstinence. Brain Res 1171:83–92.CrossRef Medline
74. Tran-Nguyen LT, Fuchs RA, Coffey GP, Baker DA, O’Dell LE, Neisewander JL (1998) Time-dependent changes in cocaine-seeking behavior and extracellular dopamine levels in the amygdala during cocaine withdrawal. Neuropsychopharmacology 19:48–59.CrossRef Medline
75. Velasquez KM, Molfese DL, Salas R (2014) The role of the habenula in drug addiction. Front Hum Neurosci 8:174.CrossRef Medline
76. Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Hitzemann R, Chen AD, Dewey SL, Pappas N (1997) Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 386:830–833.CrossRef Medline
77. Wager TD, Keller MC, Lacey SC, Jonides J (2005) Increased sensitivity in neuroimaging analyses using robust regression. Neuroimage 26:99–113.CrossRef Medline
78. Watanabe M (1996) Reward expectancy in primate prefrontal neurons. Nature 382:629–632.CrossRef Medline
79. Woicik PA, Moeller SJ, Alia-Klein N, Maloney T, Lukasik TM, Yeliosof O, Wang GJ, Volkow ND, Goldstein RZ (2009) The neuropsychology of cocaine addiction: recent cocaine use masks impairment. Neuropsychopharmacology 34:1112–1122.CrossRef Medline
80. Wu Y, Zhou X (2009) The P300 and reward valence, magnitude, and expectancy in outcome evaluation. Brain Res 1286:114–122.CrossRef Medline