Skip to main content
Log in

Prospective changes in neural alcohol cue reactivity in at-risk adolescents

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Adolescence represents an ideal time for elucidating the etiology of cue reactivity profiles. This study examined the influence of three risk factors consistently associated with heavy adolescent drinking on alcohol cue reactivity. Youth were first assessed while still naïve to alcohol (12–14 years old) and followed after transitioning into alcohol use (17–21 years old). The effects of family history of substance use disorder, sex, and history of early of dating (i.e., before 14 years of age) on BOLD response contrast to alcohol picture cues were examined in a linear mixed model, controlling for age and alcohol use patterns at follow-up. Activation to alcohol picture cues differed as a function of risk factor and time. At baseline, family history positive youth showed greater activation to alcohol cues than family history negative peers in the right middle occipital and anterior cingulate gyri. Youth with a history of early-dating showed greater activation to alcohol cues, compared to non-early daters, in the left anterior cingulate/white matter region. Girls showed greater activation to alcohol than boys at baseline in left middle frontal gyrus. At follow-up, after drinking started, patterns reversed for each risk factor. These results indicate that even prior to initiating alcohol use, adolescents showed differences in activation to alcohol cues based on their family history, dating history, and sex.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders: DSM-IV (4th ed.). Washington, DC: American Psychiatric Association.

    Google Scholar 

  • Bandettini, P. A., Jesmanowicz, A., Wong, E. C., & Hyde, J. S. (1993). Processing strategies for time-course data sets in functional MRI of the human brain. Magnetic Resonance in Medicine, 30(2), 161–173. doi:10.1002/mrm.1910300204.

    Article  PubMed  CAS  Google Scholar 

  • Bot, S. M., Engels, R. C. M. E., Knibbe, R. A., & Meeus, W. H. J. (2005). Friend's drinking behaviour and adolescent alcohol consumption: The moderating role of friendship characteristics. Addictive Behaviors, 30(5), 929–947. doi:10.1016/j.addbeh.2004.09.012.

    Article  PubMed  Google Scholar 

  • Brown, S. A., Myers, M. G., Lippke, L., Tapert, S. F., Stewart, D. G., & Vik, P. W. (1998). Psychometric evaluation of the customary drinking and drug use record (CDDR): A measure of adolescent alcohol and drug involvement. Journal of Studies on Alcohol, 59(4), 427–438. doi:10.15288/jsa.1998.59.427.

    Article  PubMed  CAS  Google Scholar 

  • Bryden, D. W., Johnson, E. E., Tobia, S. C., Kashtelyan, V., & Roesch, M. R. (2011). Attention for learning signals in anterior cingulate cortex. The Journal of Neuroscience, 31(50), 18266–18274. doi:10.1523/JNEUROSCI.4715-11.2011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cahalan, D., Cisin, I. H., & Crossley, H. M. (1969). American drinking practices: a national study of drinking behavior and attitudes. Monographs of the Rutgers Center of Alcohol Studies. New Haven: College & University Press.

  • Chartier, K. G., Hesselbrock, M. N., & Hesselbrock, V. M. (2010). Development and vulnerability factors in adolescent alcohol use. Child and Adolescent Psychiatric Clinics of North America, 19(3), 493–504. doi:10.1016/j.chc.2010.03.004.

    Article  PubMed  PubMed Central  Google Scholar 

  • Claus, E. D., Ewing, S. W., Filbey, F. M., Sabbineni, A., & Hutchison, K. E. (2011). Identifying neurobiological phenotypes associated with alcohol use disorder severity. Neuropsychopharmacology, 36(10), 2086–2096. doi:10.1038/npp.2011.99.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cohen, M. S. (1997). Parametric analysis of fMRI data using linear systems methods. NeuroImage, 6(2), 93–103.

    Article  PubMed  CAS  Google Scholar 

  • Courtney, K. E., Ghahremani, D. G., London, E. D., & Ray, L. A. (2014). The association between cue-reactivity in the precuneus and level of dependence on nicotine and alcohol. Drug and Alcohol Dependence, 141, 21–26. doi:10.1016/j.drugalcdep.2014.04.026.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173.

    Article  PubMed  CAS  Google Scholar 

  • Cox, R. W., & Jesmanowicz, A. (1999). Real-time 3D image registration for functional MRI. Magnetic Resonance in Medicine, 42, 1014–1018. doi:10.1002/(SICI)1522-2594(199912)42:6<1014::AID-MRM4>3.0.CO;2-F.

    Article  PubMed  CAS  Google Scholar 

  • Curtin, J. J., Barnett, N. P., Colby, S. M., Rohsenow, D. J., & Monti, P. M. (2005). Cue reactivity in adolescents: Measurement of separate approach and avoidance reactions. Journal of Studies on Alcohol, 66(3), 332-343, doi:10.15288/jsa.2005.66.332.

  • Dager, A. D., Anderson, B. M., Stevens, M. C., Pulido, C., Rosen, R., Jiantonio-Kelly, R. E., et al. (2013). Influence of alcohol use and family history of alcoholism on neural response to alcohol cues in college drinkers. Alcoholism, Clinical and Experimental Research, 37 Suppl 1, E161-171, doi:10.1111/j.1530-0277.2012.01879.x.

  • Dager, A. D., Anderson, B. M., Rosen, R., Khadka, S., Sawyer, B., Jiantonio-Kelly, R. E., et al. (2014). Functional magnetic resonance imaging (fMRI) response to alcohol pictures predicts subsequent transition to heavy drinking in college students. Addiction, 109(4), 585–595. doi:10.1111/add.12437.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dermen, K. H., Cooper, M. L., & Agocha, V. B. (1998). Sex-related alcohol expectancies as moderators of the relationship between alcohol use and risky sex in adolescents. Journal of Studies on Alcohol, 59(1), 71-77, doi:10.15288/jsa.1998.59.71.

  • Due, D. L., Huettel, S. A., Hall, W. G., & Rubin, D. C. (2002). Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: Evidence from functional magnetic resonance imaging. American Journal of Psychiatry, 159(6), 954–960. doi:10.1176/appi.ajp.159.6.954.

    Article  PubMed  Google Scholar 

  • Engels, R. C., & Knibbe, R. A. (2000). Alcohol use and intimate relationships in adolescence: When love comes to town. Addictive Behaviors, 25(3), 435–439. doi:10.1016/S0306-4603(98)00123-3.

    Article  PubMed  CAS  Google Scholar 

  • Erratum. (2016). Alcoholism. Clinical and Experimental Research, 40(7), 1586. doi:10.1111/acer.12793.

    Article  Google Scholar 

  • Filbey, F. M., Claus, E., Audette, A. R., Niculescu, M., Banich, M. T., Tanabe, J., et al. (2008). Exposure to the taste of alcohol elicits activation of the mesocorticolimbic neurocircuitry. Neuropsychopharmacology, 33(6), 1391–1401. doi:10.1038/sj.npp.1301513.

    Article  PubMed  CAS  Google Scholar 

  • Franken, I. H. A. (2002). Behavioral approach system (BAS) sensitivity predicts alcohol craving. Personality and Individual Differences, 32(2), 349–355. doi:10.1016/S0191-8869(01)00030-7.

    Article  Google Scholar 

  • Furman, W., Low, S., & Ho, M. J. (2009). Romantic experience and psychosocial adjustment in middle adolescence. Journal of Clinical Child and Adolescent Psychology, 38(1), 75–90. doi:10.1080/15374410802575347.

    Article  PubMed  Google Scholar 

  • Glautier, S., Bankart, J., & Williams, A. (2000). Flavour conditioning and alcohol: A multilevel model of individual differences. Biological Psychology, 52(1), 17–36. doi:10.1016/S0301-0511(99)00022-8.

    Article  PubMed  CAS  Google Scholar 

  • Goldstein, R. Z., & Volkow, N. D. (2011). Dysfunction of the prefrontal cortex in addiction: Neuroimaging findings and clinical implications. Nature Reviews Neuroscience, 12(11), 652–669. doi:10.1038/nrn3119.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goudriaan, A. E., de Ruiter, M. B., van den Brink, W., Oosterlaan, J., & Veltman, D. J. (2010). Brain activation patterns associated with cue reactivity and craving in abstinent problem gamblers, heavy smokers and healthy controls: An fMRI study. Addiction Biology, 15(4), 491–503. doi:10.1111/j.1369-1600.2010.00242.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hingson, R. W., Heeren, T., & Winter, M. R. (2006). Age at drinking onset and alcohol dependence: Age at onset, duration, and severity. Archives of Pediatrics & Adolescent Medicine, 160(7), 739–746. doi:10.1001/archpedi.160.7.739.

    Article  Google Scholar 

  • Hollingshead, A. B. (1965). Two-factor index of social position. New Haven, CT: Yale University Press.

  • Howard, D. E., & Wang, M. Q. (2003). Risk profiles of adolescent girls who were victims of dating violence. Adolescence, 38(149), 1–14.

    PubMed  Google Scholar 

  • Hyman, S. E., Malenka, R. C., & Nestler, E. J. (2006). Neural mechanisms of addiction: The role of reward-related learning and memory. Annual Review of Neuroscience, 29, 565–598. doi:10.1146/annurev.neuro.29.051605.113009.

    Article  PubMed  CAS  Google Scholar 

  • Ivory, N. J., Kambouropoulos, N., & Staiger, P. K. (2014). Cue reward salience and alcohol cue reactivity. Personality and Individual Differences, 69, 217–222. doi:10.1016/j.paid.2014.06.005.

    Article  Google Scholar 

  • Johnston, L. D., O'Malley, P. M., Miech, R. A., Bachman, J. G., & Schulenberg, J. E. (2017). Monitoring the future national survey results on drug use, 1975–2016: Overview, key findings on adolescent drug use. Ann Arbor: Institute for Social Research, The University of Michigan.

    Google Scholar 

  • Morgenstern, M., Schoeppe, F., Campbell, J., Braam, M. W., Stoolmiller, M., & Sargent, J. D. (2015). Content themes of alcohol advertising in U.S. television-latent class analysis. Alcoholism, Clinical and Experimental Research, 39(9), 1766–1774. doi:10.1111/acer.12811.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mundt, M. P. (2011). The impact of peer social networks on adolescent alcohol use initiation. Academic Pediatrics, 11(5), 414–421. doi:10.1016/j.acap.2011.05.005.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen-Louie, T. T., Castro, N., Matt, G. E., Squeglia, L. M., Brumback, T., & Tapert, S. F. (2015). Effects of emerging alcohol and marijuana use behaviors on Adolescents' neuropsychological functioning over four years. Journal of Studies on Alcohol, 76(5), 738–748. doi:10.15288/jsad. 2015.76.738.

    Article  Google Scholar 

  • Noori, H. R., Cosa Linan, A., & Spanagel, R. (2016). Largely overlapping neuronal substrates of reactivity to drug, gambling, food and sexual cues: A comprehensive meta-analysis. European Neuropsychopharmacology, 26(9), 1419–1430. doi:10.1016/j.euroneuro.2016.06.013.

    Article  PubMed  CAS  Google Scholar 

  • O'Brien, C. P., Childress, A. R., McLellan, T., & Ehrman, R. (1990). Integrating systemic cue exposure with standard treatment in recovering drug dependent patients. Addictive Behaviors, 15(4), 355–365. doi:10.1016/0306-4603(90)90045-Y.

    Article  PubMed  CAS  Google Scholar 

  • Pulido, C., Brown, S. A., Cummins, K., Paulus, M. P., & Tapert, S. F. (2010). Alcohol cue reactivity task development. Addictive Behaviors, 35(2), 84–90. doi:10.1016/j.addbeh.2009.09.006.

    Article  PubMed  Google Scholar 

  • Ray, L. A., Courtney, K. E., Hutchison, K. E., Mackillop, J., Galvan, A., & Ghahremani, D. G. (2014). Initial evidence that OPRM1 genotype moderates ventral and dorsal striatum functional connectivity during alcohol cues. Alcoholism, Clinical and Experimental Research, 38(1), 78–89. doi:10.1111/acer.12136.

    Article  PubMed  CAS  Google Scholar 

  • Rees, V. W., & Heather, N. (1995). Individual differences and cue reactivity. In D. C. Drummond, S. T. Tiffany, S. Glautier, & B. Remington (Eds.), Addictive behaviour: Cue exposure theory and practice (pp. 99–118). Oxford: John Wiley & Sons.

    Google Scholar 

  • Rice, J. P., Reich, T., Bucholz, K. K., Neuman, R. J., Fishman, R., Rochberg, N., et al. (1995). Comparison of direct interview and family history diagnoses of alcohol dependence. Alcoholism, Clinical and Experimental Research, 19(4), 1018–1023. doi:10.1111/j.1530-0277.1995.tb00983.x.

    Article  PubMed  CAS  Google Scholar 

  • Robinson, T. E., & Berridge, K. C. (1993). The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Research. Brain Research Reviews, 18(3), 247–291.

    Article  PubMed  CAS  Google Scholar 

  • Schacht, J. P., Anton, R. F., & Myrick, H. (2013). Functional neuroimaging studies of alcohol cue reactivity: A quantitative meta-analysis and systematic review. Addiction Biology, 18(1), 121–133. doi:10.1111/j.1369-1600.2012.00464.x.

    Article  PubMed  Google Scholar 

  • Seo, D., Jia, Z., Lacadie, C. M., Tsou, K. A., Bergquist, K., & Sinha, R. (2011). Sex differences in neural responses to stress and alcohol context cues. Human Brain Mapping, 32(11), 1998–2013. doi:10.1002/hbm.21165.

    Article  PubMed  Google Scholar 

  • Squeglia, L. M., Ball, T. M., Jacobus, J., Brumback, T., McKenna, B. S., Nguyen-Louie, T. T., et al. (2016). Neural predictors of initiating alcohol use during adolescence. American Journal of Psychiatry, epub ahead of print. doi:10.1176/appi.ajp.2016.15121587.

  • Stacy, A. W., Zogg, J. B., Unger, J. B., & Dent, C. W. (2004). Exposure to televised alcohol ads and subsequent adolescent alcohol use. American Journal of Health Behavior, 28(6), 498–509. doi:10.5993/AJHB.28.6.3.

    Article  PubMed  Google Scholar 

  • Swahn, M. H., Bossarte, R. M., & Sullivent, E. E. (2008). Age of alcohol use initiation, suicidal behavior, and peer and dating violence victimization and perpetration among high-risk, seventh-grade adolescents. Pediatrics, 121(2), 297–305. doi:10.1542/peds.2006-2348.

    Article  PubMed  Google Scholar 

  • Talairach, J., & Tournoux, P. (1988). Three-dimensional coplanar stereotaxic atlas of the human brain proportional system: An approach to cerebral imaging. New York: Thieme.

    Google Scholar 

  • Tapert, S. F., Cheung, E. H., Brown, G. G., Frank, L. R., Paulus, M. P., Schweinsburg, A. D., et al. (2003). Neural response to alcohol stimuli in adolescents with alcohol use disorder. Archives of General Psychiatry, 60(7), 727–735. doi:10.1001/archpsyc.60.7.727.

    Article  PubMed  Google Scholar 

  • Whelan, R., Watts, R., Orr, C. A., Althoff, R. R., Artiges, E., Banaschewski, T., et al. (2014). Neuropsychosocial profiles of current and future adolescent alcohol misusers. Nature, 512(7513), 185–189. doi:10.1038/nature13402.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • White, J. M., & Staiger, P. K. (1991). Response to alcohol cues as a function of consumption level. Drug and Alcohol Dependence, 27(2), 191–195. doi:10.1016/0376-8716(91)90039-2.

    Article  PubMed  CAS  Google Scholar 

  • van der Zwaluw, C. S., Scholte, R. H., Vermulst, A. A., Buitelaar, J., Verkes, R. J., & Engels, R. C. (2009). The crown of love: Intimate relations and alcohol use in adolescence. European Child & Adolescent Psychiatry, 18(7), 407–417. doi:10.1007/s00787-009-0748-6.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the participants, family and other informants, the San Diego Unified School District, and the outstanding research staff: Norma Castro, Claudia Cota, and Irene Lee.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susan F. Tapert.

Ethics declarations

This study was funded by the National Institutes of Health [R01 AA13419, U01 AA021692 (Tapert), F31 AA024389 (Nguyen-Louie), K12 DA031794 (Squeglia)].

Conflict of interest

All authors (TTN, KEC, LMS, KB, SE, RM, ARA, SFT, CP) of this study declare that they have no conflict of interest.

Human studies

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen-Louie, T.T., Courtney, K.E., Squeglia, L.M. et al. Prospective changes in neural alcohol cue reactivity in at-risk adolescents. Brain Imaging and Behavior 12, 931–941 (2018). https://doi.org/10.1007/s11682-017-9757-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-017-9757-0

Keywords

Navigation