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Psychopharmacology

, Volume 219, Issue 2, pp 563–573 | Cite as

Smoking withdrawal is associated with increases in brain activation during decision making and reward anticipation: a preliminary study

  • Merideth A. Addicott
  • David A. A. Baranger
  • Rachel V. Kozink
  • Moria J. Smoski
  • Gabriel S. Dichter
  • F. Joseph McClernon
Original Investigation

Abstract

Rationale

Acute nicotine abstinence is associated with disruption of executive function and reward processes; however, the neurobiological basis of these effects has not been fully elucidated.

Methods

The effects of nicotine abstinence on brain function during reward-based probabilistic decision making were preliminarily investigated by scanning adult smokers (n = 13) following 24 h of smoking abstinence and in a smoking-satiated condition. During fMRI scanning, participants completed the wheel of fortune task (Ernst et al. in Neuropsychologia 42:1585–1597, 2004), a decision-making task with probabilistic monetary outcomes. Brain activation was modeled during selection of options, anticipation of outcomes, and outcome feedback.

Results

During choice selection, reaction times were slower, and there was greater neural activation in the postcentral gyrus, insula, and frontal and parietal cortices in the abstinent condition compared to the satiated condition. During reward anticipation, greater activation was observed in the frontal pole, insula, and paracingulate cortex in the abstinent condition compared to the satiated condition. Greater activation was also shown in the precentral gyrus and putamen in the satiated condition compared to the abstinent condition. During the outcome phase, rewards (compared to no rewards) resulted in significant activation in the paracingulate cortex in the satiated condition compared to the abstinent condition.

Conclusions

The results of this preliminary study suggest that smoking withdrawal results in greater recruitment of insular, frontal, and parietal cortical areas during probabilistic decision making.

Keywords

Smoking Abstinence Decision making Risk Neuroimaging fMRI 

Notes

Acknowledgements

We thank Avery Lutz for her assistance with data acquisition. This research was supported by NIDA grants K23DA017261 and R01 DA023516 to FJM, R03 MH078145 and K23 MH081285 to GSD, and K23 MH087754 to MJS.

Disclosure/conflict of interest

Dr. Addicott, Mr. Baranger, Ms. Kozink, Dr. Smoski, and Dr. Dichter report no conflicts of interest. Dr. McClernon has received research funding from the National Institute on Drug Abuse, the Atkins Foundation, and an unrestricted grant from Philip Morris USA to Duke University (Dr. Jed E. Rose, PI).

References

  1. Baker F, Johnson MW, Bickel WK (2003) Delay discounting in current and never-before cigarette smokers: similarities and differences across commodity, sign, and magnitude. J Abnorm Psychol 112:382–392PubMedCrossRefGoogle Scholar
  2. Barry D, Petry NM (2008) Predictors of decision-making on the Iowa Gambling Task: independent effects of lifetime history of substance use disorders and performance on the Trail Making Test. Brain Cogn 66:243–252PubMedCrossRefGoogle Scholar
  3. Bechara A (2003) Risky business: emotion, decision-making, and addiction. J Gambl Stud 19:23–51PubMedCrossRefGoogle Scholar
  4. Beck A, Schlagenhauf F, Wustenberg T, Hein J, Kienast T, Kahnt T, Schmack K, Hagele C, Knutson B, Heinz A et al (2009) Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol Psychiatry 66:734–742PubMedCrossRefGoogle Scholar
  5. Bickel WK, Odum AL, Madden GJ (1999) Impulsivity and cigarette smoking: delay discounting in current, never, and ex-smokers. Psychopharmacology 146:447–454PubMedCrossRefGoogle Scholar
  6. Bickel WK, Yi R, Kowal BR, Gatchalian KM (2008) Cigarette smokers discount past and future rewards symmetrically and more than controls: is discounting a measure of impulsivity? Drug Alcohol Depend 96:256–262PubMedCrossRefGoogle Scholar
  7. Binder JR, Medler DA, Desai R, Conant LL, Liebenthal E (2005) Some neurophysiological constraints on models of word naming. Neuroimage 27:677–693PubMedCrossRefGoogle Scholar
  8. Bolla KI, Eldreth DA, London ED, Kiehl KA, Mouratidis M, Contoreggi C, Matochik JA, Kurian V, Cadet JL, Kimes AS et al (2003) Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task. Neuroimage 19:1085–1094PubMedCrossRefGoogle Scholar
  9. Brody AL, Mandelkern MA, London ED, Childress AR, Lee GS, Bota RG, Ho ML, Saxena S, Baxter LR, Madsen D et al (2002) Brain metabolic changes during cigarette craving. Arch Gen Psychiatry 59:1162–1172PubMedCrossRefGoogle Scholar
  10. Buhler M, Vollstadt-Klein S, Kobiella A, Budde H, Reed LJ, Braus DF, Buchel C, Smolka MN (2010) Nicotine dependence is characterized by disordered reward processing in a network driving motivation. Biol Psychiatry 67:745–752PubMedCrossRefGoogle Scholar
  11. Businelle MS, Kendzor DE, Rash CJ, Patterson SM, Coffey SF, Copeland AL (2009) Heavy smokers perform more poorly than nonsmokers on a simulated task of gambling. Subst Use Misuse 44:905–914PubMedCrossRefGoogle Scholar
  12. de Ruiter MB, Veltman DJ, Goudriaan AE, Oosterlaan J, Sjoerds Z, van den Brink W (2009) Response perseveration and ventral prefrontal sensitivity to reward and punishment in male problem gamblers and smokers. Neuropsychopharmacology 34:1027–1038PubMedCrossRefGoogle Scholar
  13. Dichter GS, Felder JN, Petty C, Bizzell J, Ernst M, Smoski MJ (2009) The effects of psychotherapy on neural responses to rewards in major depression. Biol Psychiatry 66:886–897PubMedCrossRefGoogle Scholar
  14. Engelmann JB, Tamir D (2009) Individual differences in risk preference predict neural responses during financial decision-making. Brain Res 1290:28–51PubMedCrossRefGoogle Scholar
  15. Epping-Jordan MP, Watkins SS, Koob GF, Markou A (1998) Dramatic decreases in brain reward function during nicotine withdrawal. Nature 393:76–79PubMedCrossRefGoogle Scholar
  16. Ernst M, Nelson EE, McClure EB, Monk CS, Munson S, Eshel N, Zarahn E, Leibenluft E, Zametkin A, Towbin K et al (2004) Choice selection and reward anticipation: an fMRI study. Neuropsychologia 42:1585–1597PubMedCrossRefGoogle Scholar
  17. Field M, Santarcangelo M, Sumnall H, Goudie A, Cole J (2006) Delay discounting and the behavioural economics of cigarette purchases in smokers: the effects of nicotine deprivation. Psychopharmacology 186:255–263PubMedCrossRefGoogle Scholar
  18. Ghahremani DG, Monterosso J, Jentsch JD, Bilder RM, Poldrack RA (2010) Neural components underlying behavioral flexibility in human reversal learning. Cereb Cortex 20:1843–1852PubMedCrossRefGoogle Scholar
  19. Gilbert DG, McClernon FJ, Rabinovich NE, Dibb WD, Plath LC, Hiyane S, Jensen RA, Meliska CJ, Estes SL, Gehlbach BA (1999) EEG, physiology, and task-related mood fail to resolve across 31 days of smoking abstinence: relations to depressive traits, nicotine exposure, and dependence. Exp Clin Psychopharmacol 7:427–443PubMedCrossRefGoogle Scholar
  20. Gilbert D, McClernon J, Rabinovich N, Sugai C, Plath L, Asgaard G, Zuo Y, Huggenvik J, Botros N (2004) Effects of quitting smoking on EEG activation and attention last for more than 31 days and are more severe with stress, dependence, DRD2 A1 allele, and depressive traits. Nicotine Tob Res 6:249–267PubMedCrossRefGoogle Scholar
  21. Harmsen H, Bischof G, Brooks A, Hohagen F, Rumpf HJ (2006) The relationship between impaired decision-making, sensation seeking and readiness to change in cigarette smokers. Addict Behav 31:581–592PubMedCrossRefGoogle Scholar
  22. Hendricks PS, Ditre JW, Drobes DJ, Brandon TH (2006) The early time course of smoking withdrawal effects. Psychopharmacology 187:385–396PubMedCrossRefGoogle Scholar
  23. Jacobsen LK, Mencl WE, Constable RT, Westerveld M, Pugh KR (2007) Impact of smoking abstinence on working memory neurocircuitry in adolescent daily tobacco smokers. Psychopharmacology 193:557–566PubMedCrossRefGoogle Scholar
  24. Koob GF (2009) Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 56:18–31PubMedCrossRefGoogle Scholar
  25. Koob GE, Le Moal M (2008) Addiction and the brain antireward system. Annu Rev Psychol 59:29–53PubMedCrossRefGoogle Scholar
  26. Kozink RV, Lutz AM, Rose JE, Froeliger B, McClernon FJ (2010) Smoking withdrawal shifts the spatiotemporal dynamics of neurocognition. Addict Biol 15:480–490PubMedCrossRefGoogle Scholar
  27. Lawrence NS, Ross TJ, Stein EA (2002) Cognitive mechanisms of nicotine on visual attention. Neuron 36:539–548PubMedCrossRefGoogle Scholar
  28. Lejuez CW, Aklin WM, Jones HA, Richards JB, Strong DR, Kahler CW, Read JP (2003) The Balloon Analogue Risk Task (BART) differentiates smokers and nonsmokers. Exp Clin Psychopharmacol 11:26–33PubMedCrossRefGoogle Scholar
  29. 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 27:4587–4597PubMedCrossRefGoogle Scholar
  30. Loughead J, Ray R, Wileyto EP, Ruparel K, Sanborn P, Siegel S, Gur RC, Lerman C (2010) Effects of the alpha4beta2 partial agonist varenicline on brain activity and working memory in abstinent smokers. Biol Psychiatry 67:715–721PubMedCrossRefGoogle Scholar
  31. Martin-Soelch C, Missimer J, Leenders KL, Schultz W (2003) Neural activity related to the processing of increasing monetary reward in smokers and nonsmokers. Eur J Neurosci 18:680–688PubMedCrossRefGoogle Scholar
  32. McClernon FJ, Kollins SH, Lutz AM, Fitzgerald DP, Murray DW, Redman C, Rose JE (2008) Effects of smoking abstinence on adult smokers with and without attention deficit hyperactivity disorder: results of a preliminary study. Psychopharmacology 197:95–105PubMedCrossRefGoogle Scholar
  33. Mendrek A, Monterosso J, Simon SL, Jarvik M, Brody A, Olmstead R, Domier CP, Cohen MS, Ernst M, London ED (2006) Working memory in cigarette smokers: comparison to non-smokers and effects of abstinence. Addict Behav 31:833–844PubMedCrossRefGoogle Scholar
  34. Mitchell SH (2004) Effects of short-term nicotine deprivation on decision-making: delay, uncertainty and effort discounting. Nicotine Tob Res 6:819–828PubMedCrossRefGoogle Scholar
  35. Myers CS, Taylor RC, Moolchan ET, Heishman SJ (2008) Dose-related enhancement of mood and cognition in smokers administered nicotine nasal spray. Neuropsychopharmacology 33:588–598PubMedCrossRefGoogle Scholar
  36. Naqvi NH, Bechara A (2009) The hidden island of addiction: the insula. Trends Neurosci 32:56–67PubMedCrossRefGoogle Scholar
  37. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531–534PubMedCrossRefGoogle Scholar
  38. Ohmura Y, Takahashi T, Kitamura N (2005) Discounting delayed and probabilistic monetary gains and losses by smokers of cigarettes. Psychopharmacology 182:508–515PubMedCrossRefGoogle Scholar
  39. Parrott AC, Garnham NJ, Wesnes K, Pincock C (1996) Cigarette smoking and abstinence: comparative effects upon cognitive task performance and mood state over 24 hours. Hum Psychopharmacol 11:391–400CrossRefGoogle Scholar
  40. Patterson F, Jepson C, Loughead J, Perkins K, Strasser AA, Siegel S, Frey J, Gur R, Lerman C (2010) Working memory deficits predict short-term smoking resumption following brief abstinence. Drug Alcohol Depend 106:61–64PubMedCrossRefGoogle Scholar
  41. Pettiford J, Kozink RV, Lutz AM, Kollins SH, Rose JE, McClernon FJ (2007) Increases in impulsivity following smoking abstinence are related to baseline nicotine intake and boredom susceptibility. Addict Behav 32:2351–2357PubMedCrossRefGoogle Scholar
  42. Powell J, Dawkins L, Davis RE (2002) Smoking, reward responsiveness, and response inhibition: tests of an incentive motivational model. Biol Psychiatry 51:151–163PubMedCrossRefGoogle Scholar
  43. Rogers RD, Ramnani N, Mackay C, Wilson JL, Jezzard P, Carter CS, Smith SM (2004) Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition. Biol Psychiatry 55:594–602PubMedCrossRefGoogle Scholar
  44. Rolls ET (2000) The orbitofrontal cortex and reward. Cereb Cortex 10:284–294PubMedCrossRefGoogle Scholar
  45. Rotheram-Fuller E, Shoptaw S, Berman SM, London ED (2004) Impaired performance in a test of decision-making by opiate-dependent tobacco smokers. Drug Alcohol Depend 73:79–86PubMedCrossRefGoogle Scholar
  46. Schoenbaum G, Setlow B, Nugent SL, Saddoris MP, Gallagher M (2003a) Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn Mem 10:129–140PubMedCrossRefGoogle Scholar
  47. Schoenbaum G, Setlow B, Ramus SJ (2003b) A systems approach to orbitofrontal cortex function: recordings in rat orbitofrontal cortex reveal interactions with different learning systems. Behav Brain Res 146:19–29PubMedCrossRefGoogle Scholar
  48. Schoenbaum G, Roesch MR, Stalnaker TA (2006) Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci 29:116–124PubMedCrossRefGoogle Scholar
  49. Shiffman SM, Jarvik ME (1976) Smoking withdrawal symptoms in two weeks of abstinence. Psychopharmacology 50:35–39PubMedCrossRefGoogle Scholar
  50. Shiffman S, Paty JA, Gnys M, Elash C, Kassel JD (1995) Nicotine withdrawal in chippers and regular smokers—subjective and cognitive effects. Health Psychol 14:301–309PubMedCrossRefGoogle Scholar
  51. Smith BW, Mitchell DGV, Hardin MG, Jazbec S, Fridberg D, Blair RJR, Ernst M (2009) Neural substrates of reward magnitude, probability, and risk during a wheel of fortune decision-making task. Neuroimage 44:600–609PubMedCrossRefGoogle Scholar
  52. Snyder FR, Davis FC, Henningfield JE (1989) The tobacco withdrawal syndrome: performance decrements assessed on a computerized test battery. Drug Alcohol Depend 23:259–266PubMedCrossRefGoogle Scholar
  53. Sweet LH, Mulligan RC, Finnerty CE, Jerskey BA, David SP, Cohen RA, Niaura RS (2010) Effects of nicotine withdrawal on verbal working memory and associated brain response. Psychiatry Res 183:69–74PubMedCrossRefGoogle Scholar
  54. Ward BD (2000) Simultaneous inference for fMRI data. Available at http://homepage.usask.ca/~ges125/fMRI/AFNIdoc/AlphaSim.pdf
  55. Xu J, Mendrek A, Cohen MS, Monterosso J, Rodriguez P, Simon SL, Brody A, Jarvik M, Domier CP, Olmstead R et al (2005) Brain activity in cigarette smokers performing a working memory task: effect of smoking abstinence. Biol Psychiatry 58:143–150PubMedCrossRefGoogle Scholar
  56. Xue G, Lu Z, Levin IP, Bechara A (2010) The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage 50:709–716PubMedCrossRefGoogle Scholar
  57. Yarkoni T, Barch DM, Gray JR, Conturo TE, Braver TS (2009) BOLD correlates of trial-by-trial reaction time variability in gray and white matter: a multi-study fMRI analysis. Plos One 4:e4257PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Merideth A. Addicott
    • 1
    • 2
  • David A. A. Baranger
    • 1
    • 2
  • Rachel V. Kozink
    • 1
    • 2
  • Moria J. Smoski
    • 1
    • 2
  • Gabriel S. Dichter
    • 1
    • 2
    • 3
  • F. Joseph McClernon
    • 1
    • 2
    • 4
  1. 1.Department of Psychiatry and Behavioral SciencesDuke University Medical CenterDurhamUSA
  2. 2.Duke-UNC Brain Imaging and Analysis CenterDurhamUSA
  3. 3.Department of Psychiatry, School of MedicineUniversity of North Carolina at Chapel HillChapel HillUSA
  4. 4.Durham Veterans Affairs Medical Center, VISN 6 Mental Illness Research, Education, and Clinical CenterDurhamUSA

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