Skip to main content
Springer Nature Link
Log in

An early attentional bias to BEGIN-stimuli of the smoking ritual is accompanied with mesocorticolimbic deactivations in smokers

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Biased processing of drug-associated stimuli is believed to be a crucial feature of addiction. Particularly, an attentional bias seems to contribute to the disorder's maintenance. Recent studies suggest differential effects for stimuli associated with the beginning (BEGIN-smoking-stimuli) or the terminal stage of the smoking ritual (END-smoking-stimuli), with the former but not the later evoking high cue-reactivity.

Objective

The current study investigated the neuronal network underlying an attentional bias to BEGIN-smoking-stimuli and END-smoking-stimuli in smokers and tested the hypothesis that the attentional bias is greater for BEGIN-smoking-stimuli.

Methods

Sixteen non-deprived smokers and 16 non-smoking controls participated in an fMRI study. Drug pictures (BEGIN-smoking-stimuli, END-smoking-stimuli) and control pictures were overlaid with geometrical figures and presented for 300 ms. Subjects had to identify picture content (identification-task) or figure orientation (distraction-task). The distraction-task was intended to demonstrate attentional bias.

Results

Behavioral data revealed an attentional bias to BEGIN-smoking-stimuli but not to END-smoking-stimuli in both groups. However, only smokers showed mesocorticolimbic deactivations in the distraction-task with BEGIN-smoking-stimuli. Importantly, these deactivations were significantly stronger for BEGIN- than for END-smoking-stimuli and correlated with the attentional bias score.

Conclusions

Several explanations may account for missing group differences in behavioral data. Brain data suggest smokers using regulatory strategies in response to BEGIN-smoking-stimuli to prevent the elicitation of motivational responses interfering with distraction-task performance. These strategies could be reflected in the observed deactivations and might lead to a performance level in smokers that is similar to that of non-smokers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
€34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Andersson JLR, Jenkinson M, Smith SM (2007a) Non-linear optimisation. FMRIB technical report TR07JA1, 2007

  • Andersson JLR, Jenkinson M, Smith SM (2007b) Non-linear registration, aka Spatial normalisation. FMRIB technical report TR07JA2, 2007

  • Attwood AS, O'Sullivan H, Leonards U, Mckintosh B, Munafò MR (2008) Attentional bias training and cue reactivity in cigarette smokers. Addiction 103:1875–1882

    Article  PubMed  Google Scholar 

  • Bechara A (2005) Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 8:1458–1463

    Article  PubMed  CAS  Google Scholar 

  • Beckmann C, Jenkinson M, Smith SM (2003) General multi-level linear modelling for group analysis in FMRI. Neuroimage 20:1052–1063

    Article  PubMed  Google Scholar 

  • Bradley MM, Lang PJ (1994) Measuring emotion: the self-assessment manikin and the semantic differential. J Behav Ther Exp Psychiatry 25:49–59

    Article  PubMed  CAS  Google Scholar 

  • Bradley MM, Cuthbert BN, Lang PJ (1993) Pictures as prepulse: attention and emotion in startle modification. Psychophysiology 30:541–545

    Article  PubMed  CAS  Google Scholar 

  • Bradley MM, Cuthbert BN, Lang PJ (1999) Affect and the startle reflex. In: Dawson ME, Schell AM, Böhmelt AH (eds) Startle modification: implications for neuroscience, cognitive science and clinical science. Cambridge University Press, pp 157–187

  • Bradley BP, Field M, Mogg K, De Houwer J (2004) Attentional and evaluative biases for smoking cues in nicotine dependence: component processes of biases in visual orienting. Behav Pharmacol 15:29–36

    Article  PubMed  CAS  Google Scholar 

  • Bradley MM, Codispoti M, Lang PJ (2006) A multi-process account of startle modulation during affective perception. Psychophysiology 43:486–497

    Article  PubMed  Google Scholar 

  • Bushnell PJ, Levin ED, Marrocco RT, Sarter MF, Strupp BJ, Warburton DM (2000) Attention as a target of intoxication: insights and methods from studies of drug abuse. Neurotoxicol Teratol 22:487–502

    Article  PubMed  CAS  Google Scholar 

  • Carter BL, Tiffany ST (1999) Meta-analysis of cue-reactivity in addiction research. Addiction 94:327–340

    Article  PubMed  CAS  Google Scholar 

  • Carter BL, Tiffany ST (2001) The cue-availability paradigm: the effects of cigarette availability on cue reactivity in smokers. Exp Clin Psychopharmacol 9:183–190

    Article  PubMed  CAS  Google Scholar 

  • Cox WM, Hogan LM, Kristian MR, Race JH (2002) Alcohol attentional bias as a predictor of alcohol abusers' treatment outcome. Drug Alcohol Depend 68:237–243

    Article  PubMed  Google Scholar 

  • Cuthbert BN, Schupp HT, Bradley MM, Birbaumer N, Lang PJ (2000) Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol Psychol 52:95–111

    Article  PubMed  CAS  Google Scholar 

  • Drobes DJ, Elibero A, Evans DE (2006) Attentional bias for smoking and affective stimuli: A Stroop task study. Psychol Addict Behav 20:490–495

    Article  PubMed  Google Scholar 

  • Ehrman RN, Robbins SJ, Bromwell MA, Lankford ME, Monterosso JR, O’Brien CP (2002) Comparing attentional bias to smoking cues in current smokers, former smokers, and non-smokers using a dot-probe task. Drug Alcohol Depend 67:185–191

    Article  PubMed  Google Scholar 

  • Ersche KD, Bullmore ET, Craig KJ, Shabbir SS, Abbott S, Müller U et al (2010) Influence of compulsivity of drug abuse on dopaminergic modulation of attentional bias in stimulant dependence. Arch Gen Psychiatry 67:632–644

    Article  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489

    Article  PubMed  CAS  Google Scholar 

  • Field M, Mogg K, Bradley BP (2004) Eye movements to smoking related cues: effects of nicotine deprivation. Psychopharmacology 173:116–123

    Article  PubMed  CAS  Google Scholar 

  • Franken IHA (2003) Drug craving and addiction: integrating psychological and neuropsychopharmacological approaches. Prog Neuropsychopharmacol Biol Psychiatry 27:563–579

    Article  PubMed  Google Scholar 

  • Geier A, Mucha RF, Pauli P (2000) Appetitive nature of drug cues confirmed with physiological measures in a model using pictures of smoking. Psychopharmacology 150:283–291

    Article  PubMed  CAS  Google Scholar 

  • Goldstein RZ, Volkow ND (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159:1642–1652

    Article  PubMed  Google Scholar 

  • Goldstein RZ, Tomasi D, Rajaram S, Cottone LA, Zhang L, Maloney T et al (2007) Role of the anterior cingulate and medial orbitofrontal cortex in processing drug cues in cocaine addiction. Neuroscience 144:1153–1159

    Article  PubMed  CAS  Google Scholar 

  • Hester R, Garavan H (2009) Neural mechanisms underlying drug-related cue distraction in active cocaine users. Pharmacol Biochem Behav 93:270–277

    Article  PubMed  CAS  Google Scholar 

  • Hindi Attar C, Andersen SK, Müller MM (2010) Time course of affective bias in visual attention: convergent evidence from steady-state visual evoked potentials and behavioral data. Neuroimage 53:1326–1333

    Article  PubMed  Google Scholar 

  • Hogarth L, Mogg K, Bradley BP, Duka T, Dickinson A (2003a) Attentional orienting towards smoking-related stimuli. Behav Pharmacol 14:153–160

    Article  PubMed  CAS  Google Scholar 

  • Hogarth L, Dickinson A, Duka T (2003b) Discriminative stimuli that control instrumental tobacco-seeking by human smokers also command selective attention. Psychopharmacology 168:435–445

    Article  PubMed  CAS  Google Scholar 

  • Huck SW, McLean RA (1975) Using a repeated measures ANOVA to analyze data from a pretest–posttest design: a potentionally confounding task. Psychol Bull 82:511–518

    Article  Google Scholar 

  • Jenkinson M (2003) A fast, automated, n-dimensional phase unwrapping algorithm. Magn Reson Med 49:193–197

    Article  PubMed  Google Scholar 

  • Jenkinson M (2004) Improving the registration of B0-disorted EPI images using calculated cost function weights. In 10th international conference on functional mapping of the human brain. June 19–22, 2004, Budapest. Available on CD-Rom in NeuroImage 20(2)

  • Jenkinson M, Smith SM (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156

    Article  PubMed  CAS  Google Scholar 

  • Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimisation for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841

    Article  PubMed  Google Scholar 

  • Kearns DN, Weiss SJ, Schindler CW, Panlilio LV (2005) Conditioned inhibition of cocaine seeking in rats. J Exp Psychol 31:247–253

    Google Scholar 

  • Lang PJ, Bradley MM, Cuthbert B (1995) International affective picture system. Center for Research in Psychophysiology, University of Florida, Gainsville, Florida

    Google Scholar 

  • LeDoux JE (2002) Synaptic self. How our brains become who we are. Penguin, New York

    Google Scholar 

  • Lubman DJ, Yücel M, Pantelis C (2004) Addiction, a condition of compulsive behaviour? Neuroimaging and neuropsychological evidence of inhibitory dysregulation. Addiction 99:1491–1502

    Article  PubMed  Google Scholar 

  • Luijten M, Veltman DJ, van den Brink W, Hester R, Field M, Smits M et al (2011) Neurobiological substrate of smoking-related attentional bias. Neuroimage 54:2374–2381

    Article  PubMed  Google Scholar 

  • McBride D, Barret SP, Kelly JT, Aw A, Dagher A (2006) Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: an fMRI study. Neuropsychopharmacology 31:2728–2738

    Article  PubMed  CAS  Google Scholar 

  • Mogg K, Bradley BP (2002) Selective processing of smoking-related cues in smokers: manipulation of deprivation level and comparison of three measures of processing bias. J Psychopharmacol 16:385–392

    Article  PubMed  Google Scholar 

  • Mogg K, Bradley BP, Field M, De Houwer J (2003) Eye movements to smoking-related pictures in smokers: relationship between attentional biases and implicit and explicit measures of stimulus valence. Addiction 98:825–836

    Article  PubMed  Google Scholar 

  • Mucha RF, Geier A, Pauli P (1999) Modulation of craving by cues having differential overlap with pharmacological effect: evidence for cue approach in smokers and social drinkers. Psychopharmacology 147:306–313

    Article  PubMed  CAS  Google Scholar 

  • Mucha RF, Pauli P, Weyers P (2006) Psychophysiology and implicit cognition in drug use: significance and measurement of motivation for drug use with emphasis on startle tests. In: Wiers RW, Stacy AW (eds) Handbook of implicit cognition and addiction. Sage Publications, Thousand Oaks, pp 201–214

    Google Scholar 

  • Mucha RF, Pauli P, Weber M, Winkler M (2008) Smoking stimuli from the terminal phase of cigarette consumption may not be cues for smoking in healthy smokers. Psychopharmacology 201:81–95

    Article  PubMed  CAS  Google Scholar 

  • Müller V, Mucha RF, Ackermann K, Pauli P (2001) Die Erfassung des Cravings bei Rauchern mit einer deutschen Version des „Questionnaire on Smoking Urges". Z Klin Psychol Psychother 30:164–171

    Article  Google Scholar 

  • Munafò M, Mogg K, Roberts S, Bradley BP, Murphy M (2003) Selective processing of smoking-related cues in current smokers, ex-smokers and never-smokers on the modified Stroop task. J Psychopharmacol 17:311–317

    Article  Google Scholar 

  • Naqvi NH, Bechara A (2009) The hidden island of addiction: the insula. Trends Neurosci 32:56–67

    Article  PubMed  CAS  Google Scholar 

  • Niaura RS, Rohsenow DJ, Binkoff JA, Monti PM, Pedraza M, Abrams DB (1988) Relevance of cue reactivity to understanding alcohol and smoking relapse. J Abnorm Psychol 97:133–152

    Article  PubMed  CAS  Google Scholar 

  • O´Brien CP, Childress AR, Ehrman R, Robbins SJ (1998) Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12:15–22

    Article  Google Scholar 

  • Panlilio LV, Thorndike EB, Schindler CW (2008) A stimulus-control account of regulated drug intake in rats. Psychopharmacology 196:441–450

    Article  PubMed  CAS  Google Scholar 

  • Penny W, Henson R (2007) Analysis of variance. In: Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE, Penny WD (eds) Statistical parametric mapping. Elsevier, Amsterdam, pp 166–177

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Robinson TE, Berridge KC (2003) Addiction. Annu Rev Psychol 54:25–53

    Article  PubMed  Google Scholar 

  • Schumann A, Rumpf HJ, Meyer C, Hapke U, John U (2003). Deutsche Version des Fagerström-Test for Nicotine Dependence (FTND-G) und des Heaviness of Smoking Index (HSI-G). In: Glöckner-Rist A, Rist F, Küfner H (eds) Elektronisches Handbuch zu Erhebungsinstrumenten im Suchtbereich (EHES). Version 3.00. Mannheim: Zentrum für Umfragen, Methoden und Analysen

  • Schupp HT, Cuthbert BN, Bradley MM, Cacioppo JT, Ito T, Lang PJ (2000) Affective picture processing: the late positive potential is modulated by motivational relevance. Psychophysiology 37:257–261

    Article  PubMed  CAS  Google Scholar 

  • Schupp HAT, Cuthbert BN, Bradley MM, Hillman CH, Hamm AO, Lang PJ (2004) Brain processes in emotional perception: motivated attention. Cognition and Emotion 18:593–611

    Article  Google Scholar 

  • Smith S (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155

    Article  PubMed  Google Scholar 

  • Stippekohl B, Winkler M, Mucha RF, Pauli P, Walter B, Vaitl D, Stark R (2010) Neural responses to BEGIN- and END-stimuli of the smoking ritual in nonsmokers, nondeprived smokers, and deprived smokers. Neuropsychopharmacology 35:1209–1255

    Article  PubMed  Google Scholar 

  • Straube T, Mentzel HJ, Miltner WHR (2006) Neural mechanisms of automatic and direct processing of phobogenic stimuli in specific phobia. Biol Psychiatry 59:162–170

    Article  PubMed  Google Scholar 

  • Volkow ND, Fowler JS, Wang GJ (2003) The addicted human brain: insights from imaging studies. J Clin Investig 111:1444–1451

    PubMed  CAS  Google Scholar 

  • Volkow ND, Fowler JS, Wang GJ (2004) The addicted human brain viewed in the light of imaging studies: brain circuits and treatment strategies. Neuropharmacology 47(S1):3–13

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Fowler JS, Wang GJ, Telang F, Logan J, Jayne M et al (2010) Cognitive control of drug craving inhibits brain reward regions in cocaine abusers. Neuroimage 49:2536–2543

    Article  PubMed  Google Scholar 

  • Waters AJ, Feyerabend C (2000) Determinants and effects of attentional bias in smokers. Psychol Addict Behav 14:111–120

    Article  PubMed  CAS  Google Scholar 

  • Waters AJ, Shiffman S, Sayette MA, Paty JA, Gwaltney CJ, Balabanis MH (2003a) Attentional bias predicts outcome in smoking cessation. Health Psychol 22:378–387

    Article  PubMed  Google Scholar 

  • Waters AJ, Shiffman S, Bradley BP, Mogg K (2003b) Attentional shifts to smoking cues in smokers. Addiction 98:1409–1417

    Article  PubMed  Google Scholar 

  • Wertz JM, Sayette MA (2001a) Effects of smoking opportunity on attentional bias in smokers. Psychol Addict Behav 15:268–271

    Article  PubMed  CAS  Google Scholar 

  • Wertz JM, Sayette MA (2001b) A review of the effects of perceived drug use opportunity on self-reported urge. Exp Clin Psychopharmacol 9:3–13

    Article  PubMed  CAS  Google Scholar 

  • Wilson SJ, Sayette MA, Fiez JA (2004) Prefrontal responses to drug cues: a neurocognitive analysis. Nat Neurosci 7:211–214

    Article  PubMed  Google Scholar 

  • Woolrich MW (2008) Robust group analysis using outlier inference. Neuroimage 41:286–301

    Article  PubMed  Google Scholar 

  • Woolrich MW, Ripley BD, Brady JM, Smith SM (2001) Temporal autocorrelation in univariate linear modelling of FMRI data. Neuroimage 14:1370–1386

    Article  PubMed  CAS  Google Scholar 

  • Woolrich MW, Behrens TEJ, Beckmann CF, Jenkinson M, Smith SM (2004) Multi-level linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21:1732–1747

    Article  PubMed  Google Scholar 

  • Worsley KJ (2001) Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM (eds) Functional MRI, an introduction to methods. Oxford University Press, pp 251–270

Download references

Acknowledgements

The study was supported by the German Research Foundation (DFG): Forschergruppe ‘Emotion and Behaviour’ (STA475/5-1) and the Graduiertenkolleg ‘NeuroAct’.

Ronald F. Mucha has in the past invested in a venture to market pictures of the end of smoking to symbolize smoking with little craving. This could be perceived as a conflict of interest, although this study was conceived and carried out independent of this. The remaining authors do not have any conflict of interest, financial or otherwise, which might bias this work.

We thank Sabine Kagerer for her indispensable language support. We further thank Sophia Rohrbeck and Annette Kroiß for assistance in data collection and analysis.

Author information

Authors and Affiliations

  1. Bender Institute of Neuroimaging, Justus-Liebig-University of Giessen, Otto-Behaghel-Str. 10H, 35394, Giessen, Germany

    Bastian Stippekohl, Bertram Walter, Dieter Vaitl & Rudolf Stark

  2. Department of Psychology, Julius-Maximilians-University of Würzburg, Marcusstraße 9-11, 97070, Würzburg, Germany

    Markus H. Winkler, Ronald F. Mucha & Paul Pauli

Authors
  1. Bastian Stippekohl
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Bertram Walter
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Markus H. Winkler
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Ronald F. Mucha
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Paul Pauli
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Dieter Vaitl
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Rudolf Stark
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Bastian Stippekohl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stippekohl, B., Walter, B., Winkler, M.H. et al. An early attentional bias to BEGIN-stimuli of the smoking ritual is accompanied with mesocorticolimbic deactivations in smokers. Psychopharmacology 222, 593–607 (2012). https://doi.org/10.1007/s00213-012-2670-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-012-2670-8

Keywords

Profiles

  1. Paul Pauli View author profile