Functional brain activation changes associated with practice in delaying smoking among moderate to heavy smokers: study protocol and rationale of a randomized trial (COPE)

Andrew T Fox, Delwyn Catley, Kimber P Richter, Edward F Ellerbeck, Morgan G Brucks, Vlad B Papa, Laura E Martin, Andrew T Fox, Delwyn Catley, Kimber P Richter, Edward F Ellerbeck, Morgan G Brucks, Vlad B Papa, Laura E Martin

Abstract

Background: Most smokers struggle to overcome tobacco addiction. Neuroscientific models of addiction emphasize the importance of brain regions associated with cognitive control and reward to understand the cycle of addiction and relapse. During an attempt at abstinence, the cognitive control system appears to be underpowered to override the heightened reward system of the addicted brain. Thus, one neural target for treatment is to strengthen the cognitive control system. It may be possible to improve the functioning of the cognitive control system via deliberate practice.

Methods/design: This study will determine the effects of practicing delaying smoking on brain and behavioral measures of cognitive control. Smoking patterns will be monitored for 1 week and then smokers (N = 80) will be randomized to either practice cognitive control by delaying their first cigarette of the day for 2 weeks (practice group) or they will continue monitoring only (no practice group). Functional magnetic resonance imaging will be performed while smokers regulate their responses to smoking images (i) at baseline and (ii) after 2 weeks of practice (or no practice).

Discussion: The primary aim of this study will be to identify the impact of practicing cognitive control on functional brain activation changes in response to smoking cues. If successful, this project will establish a neurobiological biomarker for increasing cognitive control and demonstrate the feasibility of neuroimaging methods to predict the efficacy of an intervention without a large clinical trial.

Trial registration: ClinicalTrials.gov, NCT03080844 . Registered March 15, 2017.

Keywords: Functional magnetic resonance imaging; Randomized trial; Smoking; Study protocol.

Conflict of interest statement

Ethics approval and consent to participate

All study procedures will be conducted in accordance with the Code of Ethics of the World Medical Association (Declaration of Helsinki) and have been approved by the institutional review board of the University of Kansas (protocol STUDY00004095, version 0.01).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Flow chart of enrollment, interventions, and assessments
Fig. 2
Fig. 2
Study measures and timing (SPIRIT Figure). Cigs cigarettes, MRI magnetic resonance imaging, QSU Questionnaire of Smoking Urges, UPPS-P Urgency, Premeditation, Perserverance, Sesation-Seeking, and Positive Urgencey
Fig. 3
Fig. 3
Diagram depicting scanner task

References

    1. Jamal Ahmed, King Brian A., Neff Linda J., Whitmill Jennifer, Babb Stephen D., Graffunder Corinne M. Current Cigarette Smoking Among Adults — United States, 2005–2015. MMWR. Morbidity and Mortality Weekly Report. 2016;65(44):1205–1211. doi: 10.15585/mmwr.mm6544a2.
    1. How Tobacco Smoke Causes Disease: The biology and behavioral basis for smoking-attributable disease: A report of the Surgeon General. Rockville, MD; 2010.
    1. Bechara A. Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci. 2005;8:1458–1463. doi: 10.1038/nn1584.
    1. Bickel WK, Miller ML, Yi R, Kowal BP, Lindquist DM, Pitcock JA. Behavioral and neuroeconomics of drug addiction: competing neural systems and temporal discounting processes. Drug Alcohol Depend. 2007;90(Suppl 1):S85–S91. doi: 10.1016/j.drugalcdep.2006.09.016.
    1. McClure SM, Bickel WK. A dual-systems perspective on addiction: contributions from neuroimaging and cognitive training. Ann N Y Acad Sci. 2014;1327:62–78. doi: 10.1111/nyas.12561.
    1. Baler RD, Volkow ND. Drug addiction: the neurobiology of disrupted self-control. Trends Mol Med. 2006;12:559–566. doi: 10.1016/j.molmed.2006.10.005.
    1. Koob GF, Volkow ND. Neurocircuitry of addiction. Neuropsychopharmacology. 2010;35:217–238. doi: 10.1038/npp.2009.110.
    1. Volkow ND, Wang GJ, Fowler JS, Tomasi D, Telang F, Baler R. Addiction: decreased reward sensitivity and increased expectation sensitivity conspire to overwhelm the brain's control circuit. BioEssays. 2010;32:748–755. doi: 10.1002/bies.201000042.
    1. Brody AL, Mandelkern MA, Lee G, Smith E, Sadeghi M, Saxena S, Jarvik M, London ED. Attenuation of cue-induced cigarette craving and anterior cingulate cortex activation in bupropion-treated smokers: A preliminary study. Psychiatry Res Neuroimaging. 2004;130:269–281. doi: 10.1016/j.pscychresns.2003.12.006.
    1. Ray Lara A., Courtney Kelly E., Ghahremani Dara G., Miotto Karen, Brody Arthur, London Edythe D. Varenicline, naltrexone, and their combination for heavy-drinking smokers: preliminary neuroimaging findings. The American Journal of Drug and Alcohol Abuse. 2014;41(1):35–44. doi: 10.3109/00952990.2014.927881.
    1. Culbertson CS, Bramen J, Cohen MS, London ED, Olmstead RE, Gan JJ, Costello MR, Shulenberger S, Mandelkern MA, Brody AL. Effect of bupropion treatment on brain activation induced by cigarette-related cues in smokers. Arch Gen Psychiatry. 2011;68:505–515. doi: 10.1001/archgenpsychiatry.2010.193.
    1. Franklin T, Wang Z, Suh JJ, Hazan R, Cruz J, Li Y, Goldman M, Detre JA, O'Brien CP, Childress AR. Effects of varenicline on smoking cue-triggered neural and craving responses. Arch Gen Psychiatry. 2011;68:516–526. doi: 10.1001/archgenpsychiatry.2010.190.
    1. Perkins KA, Conklin CA, Levine MD. Cognitive-Behavioral Therapy for smoking cessation: A pratical guidebook to the most effective treatments. New York: Taylor & Francis Group; 2008.
    1. Fiore MC, Jaen CR, Baker TB. Treating Tobacco Use and Dependence: 2008 Update. Rockville: U.S. Department of Health and Human Services; 2008.
    1. Lancaster T, Stead LF. Individual behavioural counselling for smoking cessation. Cochrane Database Syst Rev. 2017;(3). Art. No.: CD001292. 10.1002/14651858.CD001292.pub3.
    1. Quide Y, Witteveen AB, El-Hage W, Veltman DJ, Olff M. Differences between effects of psychological versus pharmacological treatments on functional and morphological brain alterations in anxiety disorders and major depressive disorder: a systematic review. Neurosci Biobehav Rev. 2012;36:626–644. doi: 10.1016/j.neubiorev.2011.09.004.
    1. Roiser JP, Elliott R, Sahakian BJ. Cognitive mechanisms of treatment in depression. Neuropsychopharmacology. 2012;37:117–136. doi: 10.1038/npp.2011.183.
    1. Wilson SJ, Sayett MA, Delgado MR, Fiez JA. Instructed smoking expectancy modulates cue-elicited neural activity: A preliminary study. Nicotine Tob Res. 2005;7:637–645. doi: 10.1080/14622200500185520.
    1. Due DL, Huettel SA, Hall WG, Rubin DC. Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: Evidence from functional magnetic resonance imaging. Am J Psychiatry. 2002;159:954–960. doi: 10.1176/appi.ajp.159.6.954.
    1. McClernon FJ, Hiott FB, Huettel SA, Rose JE. Abstinence-induced changes in self-report craving correlate with event-related fMRI responses to smoking cues. Neuropsychopharmacology. 2005;30:1940–1947. doi: 10.1038/sj.npp.1300780.
    1. David SP, Munafo MR, Johansen-Berg H, Smith SM, Rogers RD, Matthews PM, Walton RT. Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: A functional magnetic resonance imaging study. Biol Psychiatry. 2005;58:488–494. doi: 10.1016/j.biopsych.2005.04.028.
    1. Baker TB, Piper ME, McCarthy DE, Bolt DM, Smith SS, Kim S-Y, Colby S, Conti D, Giovino GA, Hatsukami D. Time to first cigarette in the morning as an index of ability to quit smoking: implications for nicotine dependence. Nicotine Tob Res. 2007;9:S555–S570. doi: 10.1080/14622200701673480.
    1. Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, Ochsner KN. Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci U S A. 2010;107:14811–14816. doi: 10.1073/pnas.1007779107.
    1. Engelmann JM, Versace F, Robinson JD, Minnix JA, Lam CY, Cui Y, Brown VL, Cinciripini PM. Neural substrates of smoking cue reactivity: a meta-analysis of fMRI studies. NeuroImage. 2012;60:252–262. doi: 10.1016/j.neuroimage.2011.12.024.
    1. McBride D, Barrett SP, Kelly JT, Aw A, Dagher A. Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: an fMRI study. Neuropsychopharmacology. 2006;31:2728. doi: 10.1038/sj.npp.1301075.
    1. Martin LE, Cox LS, Brooks WM, Savage CR. Winning and losing: differences in reward and punishment sensitivity between smokers and nonsmokers. Brain Behav. 2014;4:915–924. doi: 10.1002/brb3.285.
    1. Brody AL, Mandelkern MA, London ED, Childress AR, Lee GS, Bota RG, Ho ML, Saxena S, Baxter LR, Madsen D. Brain metabolic changes during cigarette craving. Arch Gen Psychiatry. 2002;59:1162–1172. doi: 10.1001/archpsyc.59.12.1162.
    1. DeGrandpre RJ, Bickel WK, Higgins ST, Hughes JR. A behavioral economic analysis of concurrently available money and cigarettes. J Exp Anal Behav. 1994;61:191–201. doi: 10.1901/jeab.1994.61-191.
    1. Martin-Sölch C, Magyar S, Künig G, Missimer J, Schultz W, Leenders K. Changes in brain activation associated with reward processing in smokers and nonsmokers. Exp Brain Res. 2001;139:278–286. doi: 10.1007/s002210100751.
    1. Martin-Soelch C, Missimer J, Leenders K, Schultz W. Neural activity related to the processing of increasing monetary reward in smokers and nonsmokers. Eur J Neurosci. 2003;18:680–688. doi: 10.1046/j.1460-9568.2003.02791.x.
    1. Carter BL, Tiffany ST. The cue-availability paradigm: the effects of cigarette availability on cue reactivity in smokers. Exp Clin Psychopharmacol. 2001;9:183–189. doi: 10.1037/1064-1297.9.2.183.
    1. McFall RM. Effects of self-monitoring on normal smoking behavior. J Consult Clin Psychol. 1970;35:135–142. doi: 10.1037/h0030087.
    1. Gilbert DG, Sugai C, Zuo Y, Eau Claire N, McClernon FJ, Rabinovich NE, Markus T, Asgaard G, Radtke R. Effects of nicotine on brain responses to emotional pictures. Nicotine Tob Res. 2004;6:985–996. doi: 10.1080/14622200410001676305.
    1. Okuyemi KS, Powell JN, Savage CR, Hall SB, Nollen N, Holsen LM, McClernon FJ, Ahluwalia JS. Enhanced cue-elicited brain activation in african american compared to caucasian smokers. Addict Biol. 2006;11:97–106. doi: 10.1111/j.1369-1600.2006.00007.x.
    1. Talairach J, Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme; 1988.
    1. Hayashi T, Ko JH, Strafella AP, Dagher A. Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving. Proc Natl Acad Sci U S A. 2013;110:4422–4427. doi: 10.1073/pnas.1212185110.
    1. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 1995;33:636–647. doi: 10.1002/mrm.1910330508.
    1. Cox RW, Chen G, Glen DR, Reynolds RC, Taylor PA. FMRI Clustering in AFNI: False-Positive Rates Redux. Brain Connectivity. 2017;7:152–171. doi: 10.1089/brain.2016.0475.
    1. Jo HJ, Gotts SJ, Reynolds RC, Bandettini PA, Martin A, Cox RW, Saad ZS. Effective preprocessing procedures virtually eliminate distance-dependent motion artifacts in resting state FMRI. J Appl Math. 2013;2013.
    1. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage. 2012;59:2142–2154. doi: 10.1016/j.neuroimage.2011.10.018.
    1. Power Jonathan D., Barnes Kelly Anne, Snyder Abraham Z., Schlaggar Bradley L., Petersen Steven E. Steps toward optimizing motion artifact removal in functional connectivity MRI; a reply to Carp. NeuroImage. 2013;76:439–441. doi: 10.1016/j.neuroimage.2012.03.017.
    1. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO. The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict. 1991;86:1119–1127. doi: 10.1111/j.1360-0443.1991.tb01879.x.
    1. COMMIT Research Group Community Intervention Trial for Smoking Cessation (COMMIT): I. Cohort results from a four-year community intervention. Am J Public Health. 1995;85:183–192. doi: 10.2105/AJPH.85.2.183.
    1. Ryan RM, Connell JP. Perceived locus of causality and internalization: examining reasons for acting in two domains. J Pers Soc Psychol. 1989;57:749–761. doi: 10.1037/0022-3514.57.5.749.
    1. Patton JH, Stanford MS, Barratt ES. Factor structure of the Barratt Impulsiveness Scale. J Clin Psychol. 1995;51:768–774. doi: 10.1002/1097-4679(199511)51:6<768::AID-JCLP2270510607>;2-1.
    1. Whiteside SP, Lynam DR, Miller JD, Reynolds SK. Validation of the UPPS impulsive behaviour scale: a four-factor model of impulsivity. Eur J Personal. 2005;19:559–574. doi: 10.1002/per.556.
    1. Torrubia R, Avila C, Moltó J, Caseras X. The Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) as a measure of Gray's anxiety and impulsivity dimensions. Personal Individ Differ. 2001;31:837–862. doi: 10.1016/S0191-8869(00)00183-5.
    1. Smith SS, Piper ME, Bolt DM, Fiore MC, Wetter DW, Cinciripini PM, Baker TB. Development of the Brief Wisconsin Inventory of Smoking Dependence Motives. Nicotine Tob Res. 2010;12:489–499. doi: 10.1093/ntr/ntq032.
    1. Kroenke K, Spitzer R, Williams J. The PHQ-9: Validity of a brief depression severity measure. J Gen Intern Med. 2001;16:606–613. doi: 10.1046/j.1525-1497.2001.016009606.x.
    1. Spitzer RL, Kroenke K, Williams JB, Löwe B. A brief measure for assessing generalized anxiety disorder: the GAD-7. Arch Intern Med. 2006;166:1092–1097. doi: 10.1001/archinte.166.10.1092.
    1. Hamilton CM, Strader LC, Pratt JG, Maiese D, Hendershot T, Kwok RK, Hammond JA, Huggins W, Jackman D, Pan H. The PhenX Toolkit: get the most from your measures. Am J Epidemiol. 2011;174:253–260. doi: 10.1093/aje/kwr193.
    1. Gearhardt AN, Corbin WR, Brownell KD. Preliminary validation of the Yale food addiction scale. Appetite. 2009;52:430–436. doi: 10.1016/j.appet.2008.12.003.
    1. Jacobs EA, Bickel WK. Modeling drug consumption in the clinic using simulation procedures: demand for heroin and cigarettes in opioid-dependent outpatients. Exp Clin Psychopharmacol. 1999;7:412. doi: 10.1037/1064-1297.7.4.412.
    1. MacKillop J, Murphy JG, Ray LA, Eisenberg DT, Lisman SA, Lum JK, Wilson DS. Further validation of a cigarette purchase task for assessing the relative reinforcing efficacy of nicotine in college smokers. Exp Clin Psychopharmacol. 2008;16:57. doi: 10.1037/1064-1297.16.1.57.
    1. Stroop JR. Studies of interference in serial verbal reactions. J Exp Psychol. 1935;18:643. doi: 10.1037/h0054651.
    1. Mueller ST, Piper BJ. The psychology experiment building language (PEBL) and PEBL test battery. J Neurosci Methods. 2014;222:250–259. doi: 10.1016/j.jneumeth.2013.10.024.
    1. Jonkman L, Lansbergen M, Stauder J. Developmental differences in behavioral and event-related brain responses associated with response preparation and inhibition in a go/nogo task. Psychophysiology. 2003;40:752–761. doi: 10.1111/1469-8986.00075.
    1. Overtoom CC, Verbaten MN, Kemner C, Kenemans JL, Van Engeland H, Buitelaar JK, Camfferman G, Koelega HS. Associations between event-related potentials and measures of attention and inhibition in the Continuous Performance Task in children with ADHD and normal controls. J Am Acad Child Adolesc Psychiatry. 1998;37:977–985. doi: 10.1097/00004583-199809000-00018.
    1. Lejuez CW, Read JP, Kahler CW, Richards JB, Ramsey SE, Stuart GL, Strong DR, Brown RA. Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART) J Exp Psychol Appl. 2002;8:75. doi: 10.1037/1076-898X.8.2.75.
    1. Mueller Shane T., Piper Brian J. The Psychology Experiment Building Language (PEBL) and PEBL Test Battery. Journal of Neuroscience Methods. 2014;222:250–259. doi: 10.1016/j.jneumeth.2013.10.024.
    1. Du W, Green L, Myerson J. Cross-cultural comparisons of discounting delayed and probabilistic rewards. Psychol Rec. 2002;52:479–492. doi: 10.1007/BF03395199.
    1. Bickel WK, Odum AL, Madden GJ. Impulsivity and cigarette smoking: delay discounting in current, never, and ex-smokers. Psychopharmacology. 1999;146:447–454. doi: 10.1007/PL00005490.
    1. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42:377–381. doi: 10.1016/j.jbi.2008.08.010.
    1. Marcus DS, Olsen TR, Ramaratnam M, Buckner RL. The Extensible Neuroimaging Archive Toolkit - An informatics platform for managing, exploring, and sharing neuroimaging data. Neuroinformatics. 2007;5:11–33. doi: 10.1385/NI:5:1:11.

Source: PubMed

3
Iratkozz fel