Skip to main content

Advertisement

SpringerLink
Log in

Sensory modality of smoking cues modulates neural cue reactivity

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

Abstract

Rationale

Behavioral experiments have demonstrated that the sensory modality of presentation modulates drug cue reactivity.

Objectives

The present study on nicotine addiction tested whether neural responses to smoking cues are modulated by the sensory modality of stimulus presentation.

Methods

We measured brain activation using functional magnetic resonance imaging (fMRI) in 15 smokers and 15 nonsmokers while they viewed images of smoking paraphernalia and control objects and while they touched the same objects without seeing them.

Results

Haptically presented, smoking-related stimuli induced more pronounced neural cue reactivity than visual cues in the left dorsal striatum in smokers compared to nonsmokers. The severity of nicotine dependence correlated positively with the preference for haptically explored smoking cues in the left inferior parietal lobule/somatosensory cortex, right fusiform gyrus/inferior temporal cortex/cerebellum, hippocampus/parahippocampal gyrus, posterior cingulate cortex, and supplementary motor area.

Conclusions

These observations are in line with the hypothesized role of the dorsal striatum for the expression of drug habits and the well-established concept of drug-related automatized schemata, since haptic perception is more closely linked to the corresponding object-specific action pattern than visual perception. Moreover, our findings demonstrate that with the growing severity of nicotine dependence, brain regions involved in object perception, memory, self-processing, and motor control exhibit an increasing preference for haptic over visual smoking cues. This difference was not found for control stimuli. Considering the sensory modality of the presented cues could serve to develop more reliable fMRI-specific biomarkers, more ecologically valid experimental designs, and more effective cue-exposure therapies of addiction.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amedi A, von Kriegstein K, van Atteveldt NM, Beauchamp MS, Naumer MJ (2005) Functional imaging of human crossmodal identification and object recognition. Exp Brain Res 166:559–571

    Article  PubMed  CAS  Google Scholar 

  • Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL (2010) Functional-anatomic fractionation of the brain's default network. Neuron 65:550–562

    Article  PubMed  CAS  Google Scholar 

  • Baler RD, Volkow ND (2006) Drug addiction: the neurobiology of disrupted self-control. Trends Mol Med 12:559–566

    Article  PubMed  CAS  Google Scholar 

  • Belin D, Everitt BJ (2008) Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57:432–441

    Article  PubMed  CAS  Google Scholar 

  • Boy F, Evans CJ, Edden RA, Singh KD, Husain M, Sumner P (2010) Individual differences in subconscious motor control predicted by GABA concentration in SMA. Curr Biol 20:1779–1785

    Article  PubMed  CAS  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 

  • Brody AL, Mandelkern MA, Olmstead RE, Jou J, Tiongson E, Allen V, Scheibal D, London ED, Monterosso JR, Tiffany ST, Korb A, Gan JJ, Cohen MS (2007) Neural substrates of resisting craving during cigarette cue exposure. Biol Psychiatry 62:642–651

    Article  PubMed  CAS  Google Scholar 

  • Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38

    Article  PubMed  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 

  • Chase HW, Eickhoff SB, Laird AR, Hogarth L (2011) The neural basis of drug stimulus processing and craving: an activation likelihood estimation meta-analysis. Biol Psychiatry 70:785–793

    Article  PubMed  Google Scholar 

  • Chua HF, Liberzon I, Welsh RC, Strecher VJ (2009) Neural correlates of message tailoring and self-relatedness in smoking cessation programming. Biol Psychiatry 65:165–168

    Article  PubMed  Google Scholar 

  • Conklin CA, Tiffany ST (2002) Applying extinction research and theory to cue-exposure addiction treatments. Addiction 97:155–167

    Article  PubMed  Google Scholar 

  • D'Ostilio K, Garraux G (2011) Automatic stimulus-induced medial premotor cortex activation without perception or action. PLoS One 6:e16613

    Article  PubMed  Google Scholar 

  • Darlow S, Lobel M (2012) Smoking behavior and motivational flexibility in light and heavy smokers. Addict Behav 37:668–673

    Article  PubMed  Google Scholar 

  • Engelmann JM, Versace F, Robinson JD, Minnix JA, Lam CY, Cui Y, Brown VL, Cinciripini PM (2012) Neural substrates of smoking cue reactivity: a meta-analysis of fMRI studies. NeuroImage 60:252–262

    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 

  • Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636–647

    Article  PubMed  CAS  Google Scholar 

  • Fowler JS, Volkow ND, Kassed CA, Chang L (2007) Imaging the addicted human brain. Sci Pract Perspect 3:4–16

    Article  PubMed  Google Scholar 

  • Franklin TR, Wang Z, Li Y, Suh JJ, Goldman M, Lohoff FW, Cruz J, Hazan R, Jens W, Detre JA, Berrettini W, O'Brien CP, Childress AR (2011) Dopamine transporter genotype modulation of neural responses to smoking cues: confirmation in a new cohort. Addict Biol 16:308–322

    Article  PubMed  CAS  Google Scholar 

  • Garavan H, Hester R (2007) The role of cognitive control in cocaine dependence. Neuropsychol Rev 17:337–345

    Article  PubMed  Google Scholar 

  • Gilbert DG, Rabinovich NE (2006) International smoking image series (with neutral counterparts). Integrative Neuroscience Laboratory, Carbondale

    Google Scholar 

  • Goebel R, Esposito F, Formisano E (2006) Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp 27:392–401

    Article  PubMed  Google Scholar 

  • Goldstein RZ, Craig AD, Bechara A, Garavan H, Childress AR, Paulus MP, Volkow ND (2009) The neurocircuitry of impaired insight in drug addiction. Trends Cogn Sci 13:372–380

    Article  PubMed  Google Scholar 

  • Grezes J, Decety J (2002) Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia 40:212–222

    Article  PubMed  CAS  Google Scholar 

  • Grezes J, Tucker M, Armony J, Ellis R, Passingham RE (2003) Objects automatically potentiate action: an fMRI study of implicit processing. Eur J Neurosci 17:2735–2740

    Article  PubMed  CAS  Google Scholar 

  • Grusser SM, Wrase J, Klein S, Hermann D, Smolka MN, Ruf M, Weber-Fahr W, Flor H, Mann K, Braus DF, Heinz A (2004) Cue-induced activation of the striatum and medial prefrontal cortex is associated with subsequent relapse in abstinent alcoholics. Psychopharmacology (Berl) 175:296–302

    Article  Google Scholar 

  • 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 86:1119–1127

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Janes AC, Smoller JW, David SP, Frederick BD, Haddad S, Basu A, Fava M, Evins AE, Kaufman MJ (2012) Association between CHRNA5 genetic variation at rs16969968 and brain reactivity to smoking images in nicotine dependent women. Drug Alcohol Depend 120:7–13

    Article  PubMed  Google Scholar 

  • Jarraya B, Brugieres P, Tani N, Hodel J, Grandjacques B, Fenelon G, Decq P, Palfi S (2010) Disruption of cigarette smoking addiction after posterior cingulate damage. J Neurosurg 113:1219–1221

    Article  PubMed  Google Scholar 

  • Jasinska AJ, Chua HF, Ho SS, Polk TA, Rozek LS, Strecher VJ (2012) Amygdala response to smoking-cessation messages mediates the effects of serotonin transporter gene variation on quitting. NeuroImage 60:766–773

    Article  PubMed  Google Scholar 

  • Johnson BA, Chen YR, Schmitz J, Bordnick P, Shafer A (1998) Cue reactivity in cocaine-dependent subjects: effects of cue type and cue modality. Addict Behav 23:7–15

    Article  PubMed  CAS  Google Scholar 

  • Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed  Google Scholar 

  • Kosten TR, Scanley BE, Tucker KA, Oliveto A, Prince C, Sinha R, Potenza MN, Skudlarski P, Wexler BE (2006) Cue-induced brain activity changes and relapse in cocaine-dependent patients. Neuropsychopharmacology 31:644–650

    Article  PubMed  CAS  Google Scholar 

  • Kotz D, Fidler J, West R (2012) Very low rate and light smokers: smoking patterns and cessation-related behaviour in England, 2006-11. Addiction 107:995–1002

    Article  PubMed  Google Scholar 

  • Kuhn S, Gallinat J (2011) Common biology of craving across legal and illegal drugs—a quantitative meta-analysis of cue-reactivity brain response. Eur J Neurosci 33:1318–1326

    Article  PubMed  Google Scholar 

  • 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) 204:25–35

    Article  CAS  Google Scholar 

  • Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9:856–869

    Article  PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Packard MG, Knowlton BJ (2002) Learning and memory functions of the basal ganglia. Annu Rev Neurosci 25:563–593

    Article  PubMed  CAS  Google Scholar 

  • Reid MS, Flammino F, Starosta A, Palamar J, Franck J (2006) Physiological and subjective responding to alcohol cue exposure in alcoholics and control subjects: evidence for appetitive responding. J Neural Transm 113:1519–1535

    Article  PubMed  CAS  Google Scholar 

  • Robbins TW, Ersche KD, Everitt BJ (2008) Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141:1–21

    Article  PubMed  CAS  Google Scholar 

  • Shadel WG, Niaura R, Abrams DB (2001) Effect of different cue stimulus delivery channels on craving reactivity: comparing in vivo and video cues in regular cigarette smokers. J Behav Ther Exp Psychiatry 32:203–209

    Article  PubMed  CAS  Google Scholar 

  • Smolka MN, Buhler M, Klein S, Zimmermann U, Mann K, Heinz A, Braus DF (2006) Severity of nicotine dependence modulates cue-induced brain activity in regions involved in motor preparation and imagery. Psychopharmacology (Berl) 184:577–588

    Article  CAS  Google Scholar 

  • Sumner P, Husain M (2008) At the edge of consciousness: automatic motor activation and voluntary control. Neuroscientist 14:474–486

    Article  PubMed  Google Scholar 

  • Sumner P, Nachev P, Morris P, Peters AM, Jackson SR, Kennard C, Husain M (2007) Human medial frontal cortex mediates unconscious inhibition of voluntary action. Neuron 54:697–711

    Article  PubMed  CAS  Google Scholar 

  • Tiffany ST (1990) A cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. Psychol Rev 97:147–168

    Article  PubMed  CAS  Google Scholar 

  • Tiffany ST, Drobes DJ (1991) The development and initial validation of a questionnaire on smoking urges. Br J Addict 86:1467–1476

    Article  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(Suppl 1):3–13

    Article  PubMed  CAS  Google Scholar 

  • Welsch SK, Smith SS, Wetter DW, Jorenby DE, Fiore MC, Baker TB (1999) Development and validation of the Wisconsin smoking withdrawal scale. Exp Clin Psychopharmacol 7:354–361

    Article  PubMed  CAS  Google Scholar 

  • Wilson SJ, Creswell KG, Sayette MA, Fiez JA (2012a) Ambivalence about smoking and cue-elicited neural activity in quitting-motivated smokers faced with an opportunity to smoke. Addict Behav

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

    Article  PubMed  Google Scholar 

  • Wilson SJ, Sayette MA, Fiez JA (2012b) Quitting-unmotivated and quitting-motivated cigarette smokers exhibit different patterns of cue-elicited brain activation when anticipating an opportunity to smoke. J Abnorm Psychol 121:198–211

    Article  PubMed  Google Scholar 

  • Wray JM, Godleski SA, Tiffany ST (2011) Cue-reactivity in the natural environment of cigarette smokers: the impact of photographic and in vivo smoking stimuli. Psychol Addict Behav 25:733–737

    Article  PubMed  Google Scholar 

  • Yalachkov Y, Kaiser J, Gorres A, Seehaus A, Naumer MJ (2012a) Smoking experience modulates the cortical integration of vision and haptics. NeuroImage 59:547–555

    Article  PubMed  Google Scholar 

  • Yalachkov Y, Kaiser J, Naumer MJ (2009) Brain regions related to tool use and action knowledge reflect nicotine dependence. J Neurosci 29:4922–4929

    Article  PubMed  CAS  Google Scholar 

  • Yalachkov Y, Kaiser J, Naumer MJ (2010) Sensory and motor aspects of addiction. Behav Brain Res 207:215–222

    Article  PubMed  Google Scholar 

  • Yalachkov Y, Kaiser J, Naumer MJ (2012b) Functional neuroimaging studies in addiction: multisensory drug stimuli and neural cue reactivity. Neurosci Biobehav Rev 36:825–835

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Hessisches Ministerium für Wissenschaft und Kultur (LOEWE Forschungsschwerpunkt Neuronale Koordination Frankfurt).

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Institute of Medical Psychology, Goethe University, Heinrich-Hoffmann-Strasse 10, 60528, Frankfurt am Main, Germany

    Yavor Yalachkov, Jochen Kaiser, Andreas Görres, Arne Seehaus & Marcus J. Naumer

Authors
  1. Yavor Yalachkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jochen Kaiser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreas Görres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arne Seehaus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marcus J. Naumer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yavor Yalachkov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yalachkov, Y., Kaiser, J., Görres, A. et al. Sensory modality of smoking cues modulates neural cue reactivity. Psychopharmacology 225, 461–471 (2013). https://doi.org/10.1007/s00213-012-2830-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-012-2830-x

Keywords

Search

Navigation