Abstract
Purpose of Review
This review aims to summarize the research on brain activity during affective processing (i.e., reward, negative emotional stimuli, loss) and adolescent substance use (SU).
Recent Findings
Most research revealed links between altered neural activity in midcingulo-insular, frontoparietal and other network regions and adolescent SU. Increased recruitment of midcingulo-insular regions—particularly the striatum —to positive affective stimuli (e.g., monetary reward) was most often associated with initiation and low-level use of substances, whereas decreased recruitment of these regions was most often associated with SUD and higher-risk SU. In regards to negative affective stimuli, most research demonstrated increased recruitment of midcingulo-insular network regions. There is also evidence that these associations may be sex-specific.
Summary
Future research should employ longitudinal designs that assess affect-related brain activity prior to and following SU initiation and escalation. Moreover, examining sex as a moderating variable may help clarify if affective neural risk factors are sex-specific.
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References
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Substance Abuse and Mental Health Services Administration, Center for Behavioral Health Statistics and Quality. The TEDS report: age of substance use initiation among treatment admissions aged 18 to 30. Rockville, MD; 2013.
Cheetham A, Allen NB, Yücel M, Lubman DI. The role of affective dysregulation in drug addiction. Clin Psychol Rev. 2010;30(6):621–34.
Colder CR, Hawk LW, Lengua LJ, Wiezcorek W, Eiden RD, Read JP. Trajectories of reinforcement sensitivity during adolescence and risk for substance use. J Res Adolesc. 2013;23(2):345–56.
Khantzian EJ. The self-medication hypothesis of substance use disorders: a reconsideration and recent applications. Harv Rev Psychiatry. 1997;4(5):231–44.
Luijten M, Schellekens AF, Kühn S, Machielse MWJ, Sescousse G. Disruption of reward processing in addiction : an image-based meta-analysis of functional magnetic resonance imaging studies. JAMA Psychiat. 2017;74(4):387–98.
Balodis IM, Potenza MN. Anticipatory reward processing in addicted populations: a focus on the monetary incentive delay task. Biol Psychiatry. 2015;77(5):434–44.
Gruber SA, Rogowska J, Yurgelun-Todd DA. Altered affective response in marijuana smokers: an FMRI study. Drug Alcohol Depend. 2009;105(1):139–53.
Casey BJ, Jones RM, Somerville LH. Braking and accelerating of the adolescent brain. J Adolesc Res. 2011;21(1):21–33.
Tervo-Clemmens B, Quach A, Calabro FJ, Foran W, Luna B. Meta-analysis and review of functional neuroimaging differences underlying adolescent vulnerability to substance use. Neuroimage. 2020;209:116476.
Uddin LQ, Yeo BTT, Spreng RN. Towards a universal taxonomy of nacro-scale functional human brain networks. Brain Topogr. 2019;32(6):926–42.
Cuthbert BN, Insel TR. Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med. 2013;11(1):126.
Crowley TJ, Dalwani MS, Mikulich-Gilbertson SK, Du YP, Lejuez CW, Raymond KM, et al. Risky Decisions and their consequences: neural processing by boys with antisocial substance disorder. PLoS One. 2010;5(9):e12835.
Dalwani MS, Tregellas JR, Andrews-Hanna JR, Mikulich-Gilbertson SK, Raymond KM, Banich MT, et al. Default mode network activity in male adolescents with conduct and substance use disorder. Drug Alcohol Depend. 2014;134:242–50.
Balleine BW, Delgado MR, Hikosaka O. The role of the dorsal striatum in reward and decision-making. J Neurosci. 2007;27(31):8161–5.
Jones SA, Cservenka A, Nagel BJ. Binge drinking impacts dorsal striatal response during decision making in adolescents. Neuroimage. 2016;129:378–88.
van Hell HH, Vink M, Ossewaarde L, Jager G, Kahn RS, Ramsey NF. Chronic effects of cannabis use on the human reward system: an fMRI study. Eur Neuropsychopharmacol. 2010;20(3):153–63.
• Claus ED, Feldstein Ewing SW, Magnan RE, Montanaro E, Hutchison KE, Bryan AD. Neural mechanisms of risky decision making in adolescents reporting frequent alcohol and/or marijuana use. Brain Imaging Behav. 2018;12(2):564–76. Provides evidence for decreased midcingulo-insular activation and substance use.
Blair RJR, Veroude K, Buitelaar JK. Neuro-cognitive system dysfunction and symptom sets: a review of fMRI studies in youth with conduct problems. Neurosci Biobehav Rev. 2018;91:69–90.
• Kim-Spoon J, Deater-Deckard K, Brieant A, Lauharatanahirun N, Lee J, King-Casas B. Brains of a feather flocking together? Peer and individual neurobehavioral risks for substance use across adolescence. Dev Psychopathol. 2019;5:1661–74. Provides evidence for altered midcingulo-insular and substance use—moderated by cognitive control.
• Elder J, Brieant A, Lauharatanahirun N, King-Casas B, Kim-Spoon J. Insular risk processing predicts alcohol use via externalizing pathway in male adolescents. J Stud Alcohol Drugs. 2019;80(6):602–13. Provides evidence for externalizing symptoms as a mediator in relation between AI and alcohol use.
Xiao L, Bechara A, Gong Q, Huang X, Li X, Xue G, et al. Abnormal affective decision making revealed in adolescent binge drinkers using a functional magnetic resonance imaging study. Psychol Addict Behav. 2013;27(2):443–54.
De Bellis MD, Wang L, Bergman SR, Yaxley RH, Hooper SR, Huettel SA. Neural mechanisms of risky decision-making and reward response in adolescent onset cannabis use disorder. Drug Alcohol Depend. 2013;133(1):134–45.
• Morales AM, Jones SA, Ehlers A, Lavine JB, Nagel BJ. Ventral striatal response during decision making involving risk and reward is associated with future binge drinking in adolescents. Neuropsychopharmacol. 2018;43(9):1884–90. Provides evidence for increased frontoparietal and occipital network activation and prospective binge drinking.
Braams BR, Peper JS, van der Heide D, Peters S, Crone EA. Nucleus accumbens response to rewards and testosterone levels are related to alcohol use in adolescents and young adults. Dev Cogn Neurosci. 2016;17:83–93.
•• Cope LM, Martz ME, Hardee JE, Zucker RA, Heitzeg MM. Reward activation in childhood predicts adolescent substance use initiation in a high-risk sample. Drug Alcohol Depend. 2019;194:318–25. Provides evidence for increased midcingulo-insular, specifically striatal, activation and SU initiation.
Stice E, Yokum S, Burger KS. Elevated reward region responsivity predicts future substance use onset but not overweight/obesity onset. Biol Psychiatry. 2013;73(9):869–76.
• Swartz JR, Weissman DG, Ferrer E, Beard SJ, Fassbender C, Robins RW, et al. Reward-related brain activity prospectively predicts increases in alcohol use in adolescents. J Am Acad Child Adolesc Psychiatry. 2020;59(3):391–400. Provides evidence for sex differences in associations between midcingulo-insular (striatal) and frontoparietal network activation and alcohol use.
Chaplin TM, Poon JA, Turpyn CC, Thompson JC (2021) Sex-differentiated pathways from negative parenting to adolescent alcohol use through stress-related neurobiology. In S. Blaine (Chair), Stress, neurobiology, and sex differences across the lifespan: identifying targets for prevention and intervention. Symposium to presented at the meeting of the Society for Research on Alcoholism, New Orleans, LA (conference cancelled due to COVID-19, paper presented virtually).
Harden KP, Mann FD, Grotzinger AD, Patterson MW, Steinberg L, Tackett JL, et al. Developmental differences in reward sensitivity and sensation seeking in adolescence: testing sex-specific associations with gonadal hormones and pubertal development. J Pers Soc Psychol. 2018;115(1):161–78.
Blum K, Cull JG, Braverman ER, Comings DE. Reward deficiency syndrome. Am Sci. 1996;84(2):132–45.
Nees F, Witt SH, Dinu-Biringer R, Lourdusamy A, Tzschoppe J, Vollstädt-Klein S, et al. BDNF Val66Met and reward-related brain function in adolescents: role for early alcohol consumption. Alcohol. 2015;49(2):103–10.
• Aloi J, Meffert H, White SF, Blair KS, Hwang S, Tyler PM, et al. Differential dysfunctions related to alcohol and cannabis use disorder symptoms in reward and error-processing neuro-circuitries in adolescents. Dev Cogn Neurosci. 2019;36:100618 . Provides evidence for altered midcingulo-insular (striatal) and occipital network activation to loss and reward and substance use.
Karoly HC, Bryan AD, Weiland BJ, Mayer A, Dodd A, Feldstein Ewing SW. Does incentive-elicited nucleus accumbens activation differ by substance of abuse? An examination with adolescents. Dev Cogn Neurosci. 2015;16:5–15.
Peters J, Bromberg U, Schneider S, Brassen S, Menz M, Banaschewski T, et al. Lower ventral striatal activation during reward anticipation in adolescent smokers. Am J Psychiatry. 2011;168(5):540–9.
•• Chaplin TM, Gonçalves SF, Poon JA, Turpyn C, Thompson JC. Sex differences in striatal response to reward predicting adolescent substance use. Provides evidence for sex differences in associations between midcingulo-insular (striatal) network activation and prospective alcohol use.
Nees F, Tzschoppe J, Patrick CJ, Vollstädt-Klein S, Steiner S, Poustka L, et al. Determinants of early alcohol use in healthy adolescents: the differential contribution of neuroimaging and psychological factors. Neuropsychopharmacol. 2012;4:986–95.
Jager G, Block RI, Luijten M, Ramsey NF. Tentative evidence for striatal hyperactivity in adolescent cannabis using boys: a cross-sectional multicenter fMRI study. J Psychoactive Drugs. 2013;45(2):156–67.
• Bertocci MA, Bebko G, Versace A, Iyengar S, Bonar L, Forbes EE, et al. Reward-related neural activity and structure predict future substance use in dysregulated youth. Psychol Med. 2017;47(8):1357–69 . Provides evidence of decreased midcingulo-insular network activation to loss and increased prospective substance use.
Pochon JB, Levy R, Fossati P, Lehericy S, Poline JB, Pillon B, Le Bihan D, Dubois B. The neural system that bridges reward and cognition in humans: an fMRI study. Proc Natl Acad Sci. 2002;99:5669–74.
de Ruiter MB, Oosterlaan J, Veltman DJ, van den Brink W, Goudriaan AE. Similar hyporesponsiveness of the dorsomedial prefrontal cortex in problem gamblers and heavy smokers during an inhibitory control task. Drug Alcohol Depend. 2012;121(1):81–9.
Vilgis V, Gelardi KL, Helm JL, Forbes EE, Hipwell AE, Keenan K, et al. Dorsomedial prefrontal activity to sadness predicts later emotion suppression and depression severity in adolescent girls. Child Dev. 2018;89(3):758–72.
Hanson JL, Hariri AR, Williamson DE. Blunted ventral striatum development in adolescence reflects emotional neglect and predicts depressive symptoms. Biol Psychiatry. 2015;78(9):598–605.
Chaplin TM, Niehaus C, Gonçalves SF. Stress reactivity and the developmental psychopathology of adolescent substance use. Neurobiol Stress. 2018;9:133–9.
Chung T, Paulsen DJ, Geier CF, Luna B, Clark DB. Regional brain activation supporting cognitive control in the context of reward is associated with treated adolescents’ marijuana problem severity at follow-up: a preliminary study. Dev Cogn Neurosci. 2015;16:93–100.
Cservenka A, Jones SA, Nagel BJ. Reduced cerebellar brain activity during reward processing in adolescent binge drinkers. Dev Cogn Neurosci. 2015;16:110–20.
Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32(1):413–34.
Brumback T, Squeglia LM, Jacobus J, Pulido C, Tapert SF, Brown SA. Adolescent heavy drinkers’ amplified brain responses to alcohol cues decrease over one month of abstinence. Addict Behav. 2015;46:45–52.
Tapert SF, Cheung EH, Brown GG, Frank LR, Paulus MP, Schweinsburg AD, et al. Neural response to alcohol stimuli in adolescents with alcohol use disorder. Arch Gen Psychiatry. 2003;60(7):727.
Yip SW, Lacadie CM, Sinha R, Mayes LC, Potenza MN. Prenatal cocaine exposure, illicit-substance use and stress and craving processes during adolescence. Drug Alcohol Depend. 2016;158:76–85.
Rubinstein ML, Luks TL, Dryden WY, Rait MA, Simpson GV. Adolescent smokers show decreased brain responses to pleasurable food images compared with nonsmokers. Nicotine Tob Res. 2011;13(8):751–5.
Migliorini R, Stewart JL, May AC, Tapert SF, Paulus MP. What do you feel? Adolescent drug and alcohol users show altered brain response to pleasant interoceptive stimuli. Drug Alcohol Depend. 2013:133(2).
Uddin LQ, Nomi JS, Hebert-Seropian B, Ghaziri J, Boucher O. Structure and function of the human insula. J Clin Neurophysiol. 2017;34(4):300–6.
• Aloi J, Blair KS, Crum KI, Meffert H, White SF, Tyler PM, et al. Adolescents show differential dysfunctions related to Alcohol and Cannabis Use Disorder severity in emotion and executive attention neuro-circuitries. Neuroimage Clin. 2018;19:782–92 . Provides evidence for altered midcingulo-insular and frontoparietal network activation and substance use.
• Leiker EK, Meffert H, Thornton LC, Taylor BK, Aloi J, Abdel-Rahim H, et al. Alcohol use disorder and cannabis use disorder symptomatology in adolescents are differentially related to dysfunction in brain regions supporting face processing. Psychiatry Res Neuroimaging. 2019;292:62–71 . Provides evidence for altered midcingulo-insular and frontoparietal network activation to reward and negative emotional stimuli and substance use.
• Elsayed NM, Kim MJ, Fields KM, Olvera RL, Hariri AR, Williamson DE. Trajectories of alcohol initiation and use during adolescence: the role of stress and amygdala reactivity. J Am Acad Child Adolesc Psychiatry. 2018;57(8):550–60 . Provides evidence for increased midcingulo-insular activation to negative emotional stimuli and substance use.
Spechler PA, Orr CA, Chaarani B, Kan K-J, Mackey S, Morton A, et al. Cannabis use in early adolescence: evidence of amygdala hypersensitivity to signals of threat. Dev Cogn Neurosci. 2015;16:63–70.
• Chaplin TM, Poon JA, Thompson JC, Hansen A, Dziura SL, Turpyn CC, et al. Sex-differentiated associations among negative parenting, emotion-related brain function, and adolescent substance use and psychopathology symptoms. Soc Dev. 2019;28(3):637–56 . Provides evidence for sex differences in midcingulo-insular network activation to negative emotional stimuli and substance use.
• May AC, Jacobus J, Stewart JL, Simmons AN, Paulus MP, Tapert SF. Do adolescents use substances to relieve uncomfortable sensations? A preliminary examination of negative reinforcement among adolescent cannabis and alcohol users. Brain Sciences. 2020;10(4):214 . Provides evidence for decreased midcingulo-insular and frontoparietal network regions to negative emotional stimuli and substance use.
Berk L, Stewart JL, May AC, Wiers RW, Davenport PW, Paulus MP, et al. Under pressure: adolescent substance users show exaggerated neural processing of aversive interoceptive stimuli. Addict. 2015;110(12):2025–36.
• Blair RJR, White SF, Tyler PM, Johnson K, Lukoff J, Thornton LC, et al. Threat responsiveness as a function of cannabis and alcohol use disorder severity. J Child Adolesc Psychopharmacol. 2019;29(7):526–34 . Provides evidence for decreased frontoparietal and occipital network activation to negative emotional stimuli and cannabis use.
•• Gonçalves SF, Turpyn CC, Niehaus CE, Mauro KL, Hinagpis CL, Thompson JC, et al. Neural activation to loss and reward among alcohol naive adolescents who later initiate alcohol use. Dev Cogn Neurosci. 2021;50:100978. Provides evidence for increased midcingulo-insular and frontoparietal network activation to loss and substance use initiation.
Funding
This research was supported in part by grants from the National Institutes of Health F31-DA051154 (PI: Gonçalves) and R01-DA033431(PI: Chaplin).
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Gonçalves, S.F., Ryan, M.P., Niehaus, C.E. et al. Affect-Related Brain Activity and Adolescent Substance Use: a Systematic Review. Curr Behav Neurosci Rep 9, 11–26 (2022). https://doi.org/10.1007/s40473-021-00241-w
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DOI: https://doi.org/10.1007/s40473-021-00241-w