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Psychopharmacology

, Volume 220, Issue 4, pp 707–718 | Cite as

Nicotine withdrawal modulates frontal brain function during an affective Stroop task

  • Brett FroeligerEmail author
  • Leslie Modlin
  • Lihong Wang
  • Rachel V. Kozink
  • F. Joseph McClernon
Original Investigation

Abstract

Background

Among nicotine-dependent smokers, smoking abstinence disrupts multiple cognitive and affective processes including conflict resolution and emotional information processing (EIP). However, the neurobiological basis of abstinence effects on resolving emotional interference on cognition remains largely uncharacterized. In this study, functional magnetic resonance imaging (fMRI) was used to investigate smoking abstinence effects on emotion–cognition interactions.

Methods

Smokers (n = 17) underwent fMRI while performing an affective Stroop task (aST) over two sessions: once following 24-h abstinence and once following smoking as usual. The aST includes trials that serially present incongruent or congruent numerical grids bracketed by neutral or negative emotional distractors and view-only emotional image trials. Statistical analyses were conducted using a statistical threshold of p < 0.05 cluster corrected.

Results

Smoking abstinence increased Stroop blood-oxygenation-level-dependent response in the right middle frontal and rostral anterior cingulate gyri. Moreover, withdrawal-induced negative affect was associated with less activation in frontoparietal regions during negative emotional information processing; whereas, during Stroop trials, negative affect predicted greater activation in frontal regions during negative, but not neutral emotional distractor trials.

Conclusion

Hyperactivation in the frontal executive control network during smoking abstinence may represent a need to recruit additional executive resources to meet task demands. Moreover, abstinence-induced negative affect may disrupt cognitive control neural circuitry during EIP and place additional demands on frontal executive neural resources during cognitive demands when presented with emotionally distracting stimuli.

Keywords

Smoking Withdrawal Emotion Affect Cognition fMRI Nicotine Stroop Cingulate PFC 

Notes

Acknowledgments

We thank Luke Poole for his assistance with data acquisition. We would also like to thank the reviewers of the manuscript for their comments and thoughtful suggestions. This research was supported by a NIDA grant R03 DA026536Z to BF.

Financial disclosures

Ms. Modlin and Ms. Kozink report no conflicts of interest. Dr. Froeliger reports having research funding from the National Institute on Drug Abuse. Dr. McClernon reports funding from the National Institute on Drug Abuse and prior funding from the Atkins Foundation and an unrestricted grant from Philip Morris USA to Duke University (Dr. Jed E. Rose, PI). Dr. Wang is supported by the Paul B. Beeson Career Developmental Awards (K23-AG028982) and a National Alliance for Research in Schizophrenia and Depression Young Investigator Award.

Supplementary material

213_2011_2522_MOESM1_ESM.doc (53 kb)
ESM 1 (DOC 53 kb)

References

  1. American Heart Association Statistics Committee and Stroke Statistics Subcommittee, Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Stafford R, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J (2010) Heart disease and stroke statistics—2010 update: a report from the American Heart Association. Circulation 121:e46–e215PubMedCrossRefGoogle Scholar
  2. APA (2000). Diagnostic and Statistical Manual of Mental Disorders DSM-IV-TR. WashingtonGoogle Scholar
  3. Asensio S, Romero MJ, Palau C, Sanchez A, Senabre I, Morales JL, Carcelen R, Romero FJ (2010) Altered neural response of the appetitive emotional system in cocaine addiction: an fMRI study. Addict Biol 15:504–516PubMedCrossRefGoogle Scholar
  4. Azizian A, Nestor LJ, Payer D, Monterosso JR, Brody AL, London ED (2010) Smoking reduces conflict-related anterior cingulate activity in abstinent cigarette smokers performing a stroop task. Neuropsychopharmacology 35:775–782PubMedCrossRefGoogle Scholar
  5. Baker TB, Piper ME, McCarthy DE, Majeskie MR, Fiore MC (2004) Addiction motivation reformulated: an affective processing model of negative reinforcement. Psychol Rev 111:33–51PubMedCrossRefGoogle Scholar
  6. Blair KS, Smith BW, Mitchell DGV, Morton J, Vythilingam M, Pessoa L, Fridberg D, Zametkin A, Nelson EE, Drevets WC, Pine DS, Martin A, Blair RJR (2007) Modulation of emotion by cognition and cognition by emotion. NeuroImage 35:430–440PubMedCrossRefGoogle Scholar
  7. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108:624–652PubMedCrossRefGoogle Scholar
  8. Botvinick MM, Cohen JD, Carter CS (2004) Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn Sci 8:539–546PubMedCrossRefGoogle Scholar
  9. Brody AL, Mandelkern MA, London ED, Childress AR, Lee GS, Bota RG, Ho ML, Saxena S, Baxter LR Jr, Madsen D, Jarvik ME (2002) Brain metabolic changes during cigarette craving. Arch Gen Psychiatry 59:1162–1172PubMedCrossRefGoogle Scholar
  10. Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215–222PubMedCrossRefGoogle Scholar
  11. Cabeza R, Nyberg L (2000) Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12:1–47PubMedCrossRefGoogle Scholar
  12. Cole DM, Beckmann CF, Long CJ, Matthews PM, Durcan MJ, Beaver JD (2010) Nicotine replacement in abstinent smokers improves cognitive withdrawal symptoms with modulation of resting brain network dynamics. NeuroImage 52:590–599PubMedCrossRefGoogle Scholar
  13. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215PubMedCrossRefGoogle Scholar
  14. Devinsky O, Morrell M, Vogt B (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306PubMedCrossRefGoogle Scholar
  15. Dolcos F, McCarthy G (2006) Brain systems mediating cognitive interference by emotional distraction. J Neurosci 26:2072–2079PubMedCrossRefGoogle Scholar
  16. Domier C, Monterosso J, Brody A, Simon S, Mendrek A, Olmstead R, Jarvik M, Cohen M, London E (2007) Effects of cigarette smoking and abstinence on stroop task performance. Psychopharmacology 195:1–9PubMedCrossRefGoogle Scholar
  17. Drevets WC (2000) Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Prog Brain Res 126:413–431PubMedCrossRefGoogle Scholar
  18. Drevets WC, Raichle ME (1998) Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: implications for interactions between emotion and cognition. Cognit Emot 12:353–385CrossRefGoogle Scholar
  19. Drobes DJ, Elibero A, Evans DE (2006) Attentional bias for smoking and affective stimuli: a Stroop task study. Psychol Addict Behav 20:490–495PubMedCrossRefGoogle Scholar
  20. Egner T, Delano M, Hirsch J (2007) Separate conflict-specific cognitive control mechanisms in the human brain. NeuroImage 35:940–948PubMedCrossRefGoogle Scholar
  21. Egner T, Etkin A, Gale S, Hirsch J (2008) Dissociable neural systems resolve conflict from emotional versus nonemotional distracters. Cereb Cortex 18:1475–1484PubMedCrossRefGoogle Scholar
  22. Etkin A, Egner T, Peraza DM, Kandel ER, Hirsch J (2006) Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 51:871–882PubMedCrossRefGoogle Scholar
  23. 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
  24. Friston KJ, Jezzard P, Turner R (1994) Analysis of functional MRI time-series. Hum Brain Mapp 1:153–171CrossRefGoogle Scholar
  25. Froeliger B, Gilbert DG, McClernon FJ (2009) Effects of nicotine on novelty detection and memory recognition performance: double-blind, placebo-controlled studies of smokers and nonsmokers. Psychopharmacology (Berl) 205(4):625–633CrossRefGoogle Scholar
  26. 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 363:3267–3276PubMedCrossRefGoogle Scholar
  27. Gilbert DG (1995) Smoking: individual difference, psychopathology, and emotion. Taylor & Francis, WashingtonGoogle Scholar
  28. Gilbert DG, Sharp JP, Ramanaiah NV, Detwiler FRJ, Anderson AE (2000) Development of a Situation × Trait Adaptive Response (STAR) model-based smoking motivation questionnaire. Personal Individ Differ 29:65–84CrossRefGoogle Scholar
  29. Gilbert DG, McClernon J, Rabinovich N, Sugai C, Plath L, Asgaard G, Zuo Y, Huggenvik J, Botros N (2004a) 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
  30. Gilbert DG, Sugai C, Zuo Y, Claire NE, McClernon FJ, Rabinovich NE, Markus T, Asgaard G, Radtke R (2004b) Effects of nicotine on brain responses to emotional pictures. Nicotine Tob Res 6:985–996PubMedCrossRefGoogle Scholar
  31. Gilbert DG, Sugai C, Zuo Y, Rabinovich NE, McClernon FJ, Froeliger B (2007) Brain indices of nicotine's effects on attentional bias to smoking and emotional pictures and to task-relevant targets. Nicotine Tob Res 9:351–363PubMedCrossRefGoogle Scholar
  32. Hart SJ, Green SR, Casp M, Belger A (2010) Emotional priming effects during Stroop task performance. Neuroimage 49:2662–2670PubMedCrossRefGoogle Scholar
  33. Hasler G, Mondillo K, Drevets WC, Blair JR (2009) Impairments of probabilistic response reversal and passive avoidance following catecholamine depletion. Neuropsychopharmacology 34:2691–2698PubMedCrossRefGoogle Scholar
  34. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO (1991) The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 86:1119–1127PubMedCrossRefGoogle Scholar
  35. Heishman S, Taylor R, Henningfield J (1994) Nicotine and smoking: a review of effects on human performance. Exp Clin Psychopharmacol 2:345–395CrossRefGoogle Scholar
  36. Hong LE, Gu H, Yang Y, Ross TJ, Salmeron BJ, Buchholz B, Thaker GK, Stein EA (2009a) Association of nicotine addiction and nicotine's actions with separate cingulate cortex functional circuits. Arch Gen Psychiatry 66:431–441PubMedCrossRefGoogle Scholar
  37. Hong LE, Schroeder M, Ross TJ, Buchholz B, Salmeron BJ, Wonodi I, Thaker GK, Stein EA (2009b) Nicotine enhances but does not normalize visual sustained attention and the associated brain network in schizophrenia. Schizophr Bull 37(2):416–425PubMedCrossRefGoogle Scholar
  38. Hooley JM, Gruber SA, Scott LA, Hiller JB, Yurgelun-Todd DA (2005) Activation in dorsolateral prefrontal cortex in response to maternal criticism and praise in recovered depressed and healthy control participants. Biol Psychiatry 57:809–812PubMedCrossRefGoogle Scholar
  39. Janes AC, Pizzagalli DA, Richardt S, Frederick BD, Chuzi S, Pachas G, Culhane MA, Holmes AJ, Fava M, Evins AE, Kaufman MJ (2010) Brain reactivity to smoking cues prior to smoking cessation predicts ability to maintain tobacco abstinence. Biol Psychiatry 67:722–729PubMedCrossRefGoogle Scholar
  40. Japuntich SJ, Smith SS, Jorenby DE, Piper ME, Fiore MC, Baker TB (2007) Depression predicts smoking early but not late in a quit attempt. Nicotine Tob Res 9:677–686PubMedCrossRefGoogle Scholar
  41. Kemmotsu N, Villalobos ME, Gaffrey MS, Courchesne E, Müller R-A (2005) Activity and functional connectivity of inferior frontal cortex associated with response conflict. Brain Res Cogn Brain Res 24:335–342PubMedCrossRefGoogle Scholar
  42. Kerns JG, Cohen JD, MacDonald AW, Cho RY, Stenger VA, Carter CS (2004) Anterior cingulate conflict monitoring and adjustments in control. Science 303:1023–1026PubMedCrossRefGoogle Scholar
  43. Kim C, Kroger JK, Kim J (2011) A functional dissociation of conflict processing within anterior cingulate cortex. Hum Brain Mapp 32:304–312PubMedCrossRefGoogle Scholar
  44. Knott V, Bosman M, Mahoney C, Ilivitsky V, Quirt K (1999) Transdermal nicotine: single dose effects on mood, EEG, performance, and event-related potentials. Pharmacol Biochem Behav 63:253–261PubMedCrossRefGoogle Scholar
  45. Koob GF, Le Moal M (2008) Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B Biol Sci 363:3113–3123PubMedCrossRefGoogle Scholar
  46. Koob GF, Volkow ND (2009) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238CrossRefGoogle Scholar
  47. Kozink RV, Kollins SH, McClernon FJ (2010a) Smoking withdrawal modulates right inferior frontal cortex but not presupplementary motor area activation during inhibitory control. Neuropsychopharmacology 35:2600–2606PubMedCrossRefGoogle Scholar
  48. Kozink RV, Lutz AM, Rose JE, Froeliger B, McClernon FJ (2010b) Smoking withdrawal shifts the spatiotemporal dynamics of neurocognition. Addict Biol 15:480–490PubMedCrossRefGoogle Scholar
  49. Krall EA, Garvey AJ, Garcia RI (2002) Smoking relapse after 2 years of abstinence: findings from the VA Normative Aging Study. Nicotine Tob Res 4:95–100PubMedCrossRefGoogle Scholar
  50. Lang PJ, Bradley MM, Cuthbert BN (1997) International Affective Picture System (IAPS). NIMH Center for the Study of Emotion and Attention, GainesvilleGoogle Scholar
  51. London ED, Simon SL, Berman SM, Mandelkern MA, Lichtman AM, Bramen J, Shinn AK, Miotto K, Learn J, Dong Y, Matochik JA, Kurian V, Newton T, Woods R, Rawson R, Ling W (2004) Mood disturbances and regional cerebral metabolic abnormalities in recently abstinent methamphetamine abusers. Arch Gen Psychiatry 61:73–84PubMedCrossRefGoogle Scholar
  52. Loughead J, Wileyto EP, Valdez JN, Sanborn P, Tang K, Strasser AA, Ruparel K, Ray R, Gur RC, Lerman C (2009) Effect of abstinence challenge on brain function and cognition in smokers differs by COMT genotype. Mol Psychiatry 14:820–826PubMedCrossRefGoogle Scholar
  53. Mathews A, MacLeod C (1985) Selective processing of threat cues in anxiety states. Behav Res Ther 23:563–569PubMedCrossRefGoogle Scholar
  54. Mayberg HS (1997) Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci 9:471–481PubMedGoogle Scholar
  55. McClernon FJ, Hiott FB, Huettel SA, Rose JE (2005) Abstinence-induced changes in self-report craving correlate with event-related fMRI responses to smoking cues. Neuropsychopharmacology 30:1940–1947PubMedCrossRefGoogle Scholar
  56. McClernon F, Kollins S, Lutz A, Fitzgerald D, Murray D, Redman C, Rose J (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
  57. McClernon FJ, Kozink RV, Lutz AM, Rose JE (2009) 24-h smoking abstinence potentiates fMRI-BOLD activation to smoking cues in cerebral cortex and dorsal striatum. Psychopharmacology (Berl) 204:25–35CrossRefGoogle Scholar
  58. 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
  59. Mincic AM (2010) Neural substrate of the cognitive and emotional interference processing in healthy adolescents. Acta Neurobiol Exp 70:406–422Google Scholar
  60. Mueller-Pfeiffer C, Martin-Soelch C, Blair JR, Carnier A, Kaiser N, Rufer M, Schnyder U, Hasler G (2010) Impact of emotion on cognition in trauma survivors: what is the role of posttraumatic stress disorder? J Affect Disord 126:287–292PubMedCrossRefGoogle Scholar
  61. Nee DE, Jonides J, Berman MG (2007a) Neural mechanisms of proactive interference-resolution. NeuroImage 38:740–751PubMedCrossRefGoogle Scholar
  62. Nee DE, Wager TD, Jonides J (2007b) Interference resolution: insights from a meta-analysis of neuroimaging tasks. Cogn Affect Behav Neurosci 7:1–17PubMedCrossRefGoogle Scholar
  63. Ochsner KN, Gross JJ (2008) Cognitive emotion regulation: insights from social cognitive and affective neuroscience. Curr Dir Psychol Sci 17:153–158CrossRefGoogle Scholar
  64. Ochsner KN, Bunge SA, Gross JJ, Gabrieli JD (2002) Rethinking feelings: an FMRI study of the cognitive regulation of emotion. J Cogn Neurosci 14:1215–1229PubMedCrossRefGoogle Scholar
  65. Ochsner KN, Ray RD, Cooper JC, Robertson ER, Chopra S, Gabrieli JDE, Gross JJ (2004) For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23:483–499PubMedCrossRefGoogle Scholar
  66. Pansky A, Algom D (2002) Comparative judgment of numerosity and numerical magnitude: attention preempts automaticity. J Exp Psychol Learn Mem Cogn 28:259–274PubMedCrossRefGoogle Scholar
  67. 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 Clin Exp 11:391–400CrossRefGoogle Scholar
  68. 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
  69. Piper ME, Cook JW, Schlam TR, Jorenby DE, Baker TB (2011) Anxiety diagnoses in smokers seeking cessation treatment: relations with tobacco dependence, withdrawal, outcome and response to treatment. Addiction 106:418–427PubMedCrossRefGoogle Scholar
  70. Radloff LS (1977) The CES-D scale: a self report depression scale for research in the general population. Appl Psychol Meas 1:385–401CrossRefGoogle Scholar
  71. Rose JE, Behm FM, Westman EC, Mathew RJ, London ED, Hawk TC, Turkington TG, Coleman RE (2003) PET studies of the influences of nicotine on neural systems in cigarette smokers. Am J Psychiatry 160:323–333PubMedCrossRefGoogle Scholar
  72. Rzetelny A, Gilbert DG, Hammersley J, Radtke R, Rabinovich NE, Small SL (2008) Nicotine decreases attentional bias to negative-affect-related Stroop words among smokers. Nicotine Tob Res 10:1029–1036PubMedCrossRefGoogle Scholar
  73. Salo R, Ursu S, Buonocore MH, Leamon MH, Carter C (2009) Impaired prefrontal cortical function and disrupted adaptive cognitive control in methamphetamine abusers: a functional magnetic resonance imaging study. Biol Psychiatry 65:706–709PubMedCrossRefGoogle Scholar
  74. Shiffman SM, Jarvik ME (1976) Smoking withdrawal symptoms in 2 weeks of abstinence. Psychopharmacology 50:35–39PubMedCrossRefGoogle Scholar
  75. Shiffman S, Waters AJ (2004) Negative affect and smoking lapses: a prospective analysis. J Consult Clin Psychol 72:192–201PubMedCrossRefGoogle Scholar
  76. Shiffman S, Shumaker SA, Abrams DB, Cohen S, Garvey A, Grunberg NE, Swan GE (1986) Models of smoking relapse. Health Psychol 5(Suppl):13–27PubMedCrossRefGoogle Scholar
  77. Siegle GJ, Steinhauer SR, Thase ME, Stenger VA, Carter CS (2002) Can't shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 51:693–707PubMedCrossRefGoogle Scholar
  78. Siegle GJ, Thompson W, Carter CS, Steinhauer SR, Thase ME (2007) Increased amygdala and decreased dorsolateral prefrontal bold responses in unipolar depression: related and independent features. Biol Psychiatry 61:198–209PubMedCrossRefGoogle Scholar
  79. Spielberger CD (1986) Psychological determinants of smoking behavior. In: Tollinson RD (ed) Smoking and society: toward a more balanced assessment. Heath, LexingtonGoogle Scholar
  80. Stein EA, Pankiewicz J, Harsch HH, Cho J-K, Fuller SA, Hoffmann RG, Hawkins M, Rao SM, Bandettini PA, Bloom AS (1998) Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiatry 155:1009–1015PubMedGoogle Scholar
  81. Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 28:643–662CrossRefGoogle Scholar
  82. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289PubMedCrossRefGoogle Scholar
  83. Verdejo-Garcia A, Perez-Garcia M, Bechara A (2006) Emotion, decision-making and substance dependence: a somatic-marker model of addiction. Curr Neuropharmacol 4:17–31PubMedCrossRefGoogle Scholar
  84. Vythilingam M, Blair KS, McCaffrey D, Scaramozza M, Jones M, Nakic M, Mondillo K, Hadd K, Bonne O, Mitchell DG, Pine DS, Charney DS, Blair RJ (2007) Biased emotional attention in post-traumatic stress disorder: a help as well as a hindrance? Psychol Med 37:1445–1455PubMedCrossRefGoogle Scholar
  85. Walter B, Blecker C, Kirsch P, Sammer G, Schienle A, Stark R, Vaitl D (2003). MARINA: An easy to use tool for the creation of MAsks for Region of INterest Analyses [abstract]. In 9th International Conference on Functional Mapping of the Human Brain, New YorkGoogle Scholar
  86. Wang L, LaBar KS, Smoski M, Rosenthal MZ, Dolcos F, Lynch TR, Krishnan RR, McCarthy G (2008) Prefrontal mechanisms for executive control over emotional distraction are altered in major depression. Psychiatry Res 163:143–155PubMedCrossRefGoogle Scholar
  87. Ward B (2000) Simultaneous inference for fMRI data. Biophysics Research Institute, Medical College of Wisconsin, MilwaukeeGoogle Scholar
  88. Whalen PJ, Bush G, McNally RJ, Wilhelm S, McInerney SC, Jenike MA, Rauch SL (1998) The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division. Biol Psychiatry 44:1219–1228PubMedCrossRefGoogle Scholar
  89. Xu J, Mendrek A, Cohen MS, Monterosso J, Rodriguez P, Simon SL, Brody A, Jarvik M, Domier CP, Olmstead R, Ernst M, London ED (2005) Brain activity in cigarette smokers performing a working memory task: effect of smoking abstinence. Biol Psychiatry 58:143–150PubMedCrossRefGoogle Scholar
  90. Xu J, Mendrek A, Cohen MS, Monterosso J, Simon S, Brody AL, Jarvik M, Rodriguez P, Ernst M, London ED (2006) Effects of acute smoking on brain activity vary with abstinence in smokers performing the N-Back Task: a preliminary study. Psychiatry Res 148:103–109PubMedCrossRefGoogle Scholar
  91. Yamasaki H, LaBar KS, McCarthy G (2002) Dissociable prefrontal brain systems for attention and emotion. Proc Natl Acad Sci U S A 99:11447–11451PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Brett Froeliger
    • 1
    • 2
    Email author
  • Leslie Modlin
    • 3
    • 4
  • Lihong Wang
    • 4
    • 5
  • Rachel V. Kozink
    • 3
    • 4
  • F. Joseph McClernon
    • 3
    • 4
    • 6
  1. 1.Department of Psychiatry and Behavioral SciencesDuke University Medical CenterDurhamUSA
  2. 2.Department of Psychiatry and Behavioral SciencesDuke-UNC Brain Imaging and Analysis CenterDurhamUSA
  3. 3.Department of Psychiatry and Behavioral SciencesDuke University Medical CenterDurhamUSA
  4. 4.Duke-UNC Brain Imaging and Analysis CenterDurhamUSA
  5. 5.Department of Psychiatry and Behavioral SciencesDuke University Medical CenterDurhamUSA
  6. 6.VISN 6 Mental Illness Research, Education, and Clinical CenterDurham Veterans Affairs Medical CenterDurhamUSA

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