Abstract
Objective: It is unclear whether deviations in brain and behavioral development, which may underpin elevated substance use during adolescence, are predispositions for or consequences of substance use initiation. Here, we examine behavioral and neuroimaging indices at early and mid-adolescence in drug-naive youths to identify possible predisposing factors for substance use initiation and its possible consequences. Method: Among 304 drug-naive adolescents at baseline (age 14 years) from the IMAGEN dataset, 83 stayed drug-naive, 133 used alcohol on 1 to 9 occasions, 42 on 10 to 19 occasions, 27 on 20 to 39 occasions, and 19 on >40 occasions at follow-up (age 16 years). Baseline measures included brain activation during the Monetary Incentive Delay task. Data at both baseline and follow-up included measures of trait impulsivity and delay discounting. Results: From baseline to follow-up, impulsivity decreased in the 0 and 1- to 9-occasions groups (p < .004), did not change in the 10- to 19-occasions and 20- to 29-occasions groups (p > .294), and uncharacteristically increased in the >40-occasions group (p = .046). Furthermore, blunted medial orbitofrontal cortex activation during reward outcome at baseline significantly predicted higher alcohol use frequency at follow-up, above and beyond behavioral and clinical variables (p = .008). Conclusion: These results suggest that the transition from no use to frequent drinking in early to mid-adolescence may disrupt normative developmental changes in behavioral control. In addition, blunted activity of the medial orbitofrontal cortex during reward outcome may underscore a predisposition toward the development of more severe alcohol use in adolescents. This distinction is clinically important, as it informs early intervention efforts in preventing the onset of substance use disorder in adolescents.
Original language | English |
---|---|
Pages (from-to) | 623-636 |
Number of pages | 14 |
Journal | Journal of the American Academy of Child and Adolescent Psychiatry |
Volume | 60 |
Issue number | 5 |
DOIs | |
Publication status | Published - May 2021 |
Keywords
- adolescence
- alcohol use
- IMAGEN
- impulsivity
- reward processing
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In: Journal of the American Academy of Child and Adolescent Psychiatry, Vol. 60, No. 5, 05.2021, p. 623-636.
Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Substance Use Initiation, Particularly Alcohol, in Drug-Naive Adolescents
T2 - Possible Predictors and Consequences From a Large Cohort Naturalistic Study
AU - IMAGEN Consortium
AU - Ivanov, Iliyan
AU - Parvaz, Muhammad A.
AU - Velthorst, Eva
AU - Shaik, Riaz B.
AU - Sandin, Sven
AU - Gan, Gabriela
AU - Spechler, Philip
AU - Albaugh, Matthew D.
AU - Chaarani, Bader
AU - Mackey, Scott
AU - Banaschewski, Tobias
AU - Bokde, Arun L.W.
AU - Bromberg, Uli
AU - Büchel, Christian
AU - Burke Quinlan, Erin
AU - Desrivieres, Sylvane
AU - Flor, Herta
AU - Grigis, Antoine
AU - Gowland, Penny
AU - Heinz, Andreas
AU - Ittermann, Bernd
AU - Martinot, Jean Luc
AU - Paillère Martinot, Marie Laure
AU - Artiges, Eric
AU - Lemaitre, Herve
AU - Nees, Frauke
AU - Orfanos, Dimitri Papadopoulos
AU - Paus, Tomáš
AU - Schumann, Gunter
AU - Barker, Gareth
AU - Cattrell, Anna
AU - Jia, Tianye
AU - Conrod, Patricia
AU - Desrivieres, Sylvane
AU - Mallik, Catherine
AU - Martinez-Medina, Lourdes
AU - Nymberg, Charlotte
AU - Biondo, Francesca
AU - Struve, Maren
AU - Williams, Steve
AU - Rogers, John
AU - Ing, Alex
AU - Ruggeri, Barbara
AU - Xu, Bing
AU - Macare, Christine
AU - Chu, Congying
AU - Hanratty, Eanna
AU - Burke Quinlan, Erin
AU - Robert, Gabriel
AU - Yu, Tao
N1 - Funding Information: This work received support from the following sources: the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT- 2007-037286), the Horizon 2020 funded ERC Advanced Grant ‘STRATIFY’ (Brain network based stratification of reinforcement-related disorders) (695313), Human Brain Project (HBP SGA 2, 785907, and HBP SGA 3, 945539), the Medical Research Council Grant 'c-VEDA’ (Consortium on Vulnerability to Externalizing Disorders and Addictions) (MR/N000390/1), the National Institute of Health (NIH) (R01DA049238, A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers), the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, the Bundesministeriumfür Bildung und Forschung (BMBF grants 01GS08152; 01EV0711; Forschungsnetz AERIAL 01EE1406A, 01EE1406B), the Deutsche Forschungsgemeinschaft (DFG grants SM 80/7-2, SFB 940, TRR 265, NE 1383/14-1), the Medical Research Foundation and Medical Research Council (grants MR/R00465X/1 and MR/S020306/1), and the National Institutes of Health (NIH) funded ENIGMA (grants 5U54EB020403-05 and 1R56AG058854-01). Further support was provided by grants from: the ANR (ANR-12-SAMA-0004, AAPG2019 - GeBra), the Eranet Neuron (AF12-NEUR0008-01 - WM2NA; and ANR-18-NEUR00002-01 - ADORe), the Fondation de France (00081242), the Fondation pour la Recherche Médicale (DPA20140629802), the Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA), the Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant), Paris Sud University IDEX 2012, the Fondation de l’Avenir (grant AP-RM-17-013 ), the Fédération pour la Recherche sur le Cerveau; the National Institutes of Health , Science Foundation Ireland (16/ERCD/3797), U.S.A. (Axon, Testosterone and Mental Health during Adolescence; RO1 MH085772-01A1), and by NIH Consortium grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence. Additional funding from the NIH includes KL2TR001435 and K01DA043615 to M.A.P. and R01MH085772 to T.P. E.V. is supported by the Seaver Research Foundation and NARSAD Young Investigator Award from the Brain and Behavior Foundation. Funding Information: This work received support from the following sources: the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT- 2007-037286), the Horizon 2020 funded ERC Advanced Grant ?STRATIFY? (Brain network based stratification of reinforcement-related disorders) (695313), Human Brain Project (HBP SGA 2, 785907, and HBP SGA 3, 945539), the Medical Research Council Grant 'c-VEDA? (Consortium on Vulnerability to Externalizing Disorders and Addictions) (MR/N000390/1), the National Institute of Health (NIH) (R01DA049238, A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers), the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London, the Bundesministeriumf?r Bildung und Forschung (BMBF grants 01GS08152; 01EV0711; Forschungsnetz AERIAL 01EE1406A, 01EE1406B), the Deutsche Forschungsgemeinschaft (DFG grants SM 80/7-2, SFB 940, TRR 265, NE 1383/14-1), the Medical Research Foundation and Medical Research Council (grants MR/R00465X/1 and MR/S020306/1), and the National Institutes of Health (NIH) funded ENIGMA (grants 5U54EB020403-05 and 1R56AG058854-01). Further support was provided by grants from: the ANR (ANR-12-SAMA-0004, AAPG2019 - GeBra), the Eranet Neuron (AF12-NEUR0008-01 - WM2NA; and ANR-18-NEUR00002-01 - ADORe), the Fondation de France (00081242), the Fondation pour la Recherche M?dicale (DPA20140629802), the Mission Interminist?rielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA), the Assistance-Publique-H?pitaux-de-Paris and INSERM (interface grant), Paris Sud University IDEX 2012, the Fondation de l'Avenir (grant AP-RM-17-013 ), the F?d?ration pour la Recherche sur le Cerveau; the National Institutes of Health, Science Foundation Ireland (16/ERCD/3797), U.S.A. (Axon, Testosterone and Mental Health during Adolescence; RO1 MH085772-01A1), and by NIH Consortium grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence. Additional funding from the NIH includes KL2TR001435 and K01DA043615 to M.A.P. and R01MH085772 to T.P. E.V. is supported by the Seaver Research Foundation and NARSAD Young Investigator Award from the Brain and Behavior Foundation.ImagenPathways ?Understanding the Interplay between Cultural, Biological and Subjective Factors in Drug Use Pathways? is a collaborative project supported by the European Research Area Network on Illicit Drugs (ERANID). This paper is based on independent research commissioned and funded in England by the National Institute for Health Research (NIHR) Policy Research Programme (project ref. PR-ST-0416-10001). The views expressed in this article are those of the authors and not necessarily those of the national funding agencies or ERANID.Disclosure: Dr. Banaschewski has served in an advisory or consultancy role for Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, and Shire (a Takeda company). He has received conference support or speaker's fee by Eli Lilly and Co., Medice, Novartis, and Shire. He has been involved in clinical trials conducted by Shire and Viforpharma. He has received royalties from Hogrefe, Kohlhammer, CIP Medien, and Oxford University Press. Drs. Ivanov, Parvaz, Velthorst, Shaik, Sandin, Gan, Spechler, Albaugh, Chaarani, Mackey, Bokde, Bromberg, B?chel, Burke Quinlan, Desrivi?res, Flor, Grigis, Gowland, Heinz, Ittermann, Martinot, Paill?re Martinot, Artiges, Lemaitre, Nees, Papadopoulos Orfanos, Paus, Poustka, Hohmann, Millenet, Fr?hner, Smolka, Walter, Whelan, Schumann, and Garavan have reported no biomedical financial interests or potential conflicts of interest. Funding Information: ImagenPathways “Understanding the Interplay between Cultural, Biological and Subjective Factors in Drug Use Pathways” is a collaborative project supported by the European Research Area Network on Illicit Drugs (ERANID). This paper is based on independent research commissioned and funded in England by the National Institute for Health Research (NIHR) Policy Research Programme (project ref. PR-ST-0416-10001). The views expressed in this article are those of the authors and not necessarily those of the national funding agencies or ERANID. Publisher Copyright: © 2020 American Academy of Child and Adolescent Psychiatry Copyright: Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2021/5
Y1 - 2021/5
N2 - Objective: It is unclear whether deviations in brain and behavioral development, which may underpin elevated substance use during adolescence, are predispositions for or consequences of substance use initiation. Here, we examine behavioral and neuroimaging indices at early and mid-adolescence in drug-naive youths to identify possible predisposing factors for substance use initiation and its possible consequences. Method: Among 304 drug-naive adolescents at baseline (age 14 years) from the IMAGEN dataset, 83 stayed drug-naive, 133 used alcohol on 1 to 9 occasions, 42 on 10 to 19 occasions, 27 on 20 to 39 occasions, and 19 on >40 occasions at follow-up (age 16 years). Baseline measures included brain activation during the Monetary Incentive Delay task. Data at both baseline and follow-up included measures of trait impulsivity and delay discounting. Results: From baseline to follow-up, impulsivity decreased in the 0 and 1- to 9-occasions groups (p < .004), did not change in the 10- to 19-occasions and 20- to 29-occasions groups (p > .294), and uncharacteristically increased in the >40-occasions group (p = .046). Furthermore, blunted medial orbitofrontal cortex activation during reward outcome at baseline significantly predicted higher alcohol use frequency at follow-up, above and beyond behavioral and clinical variables (p = .008). Conclusion: These results suggest that the transition from no use to frequent drinking in early to mid-adolescence may disrupt normative developmental changes in behavioral control. In addition, blunted activity of the medial orbitofrontal cortex during reward outcome may underscore a predisposition toward the development of more severe alcohol use in adolescents. This distinction is clinically important, as it informs early intervention efforts in preventing the onset of substance use disorder in adolescents.
AB - Objective: It is unclear whether deviations in brain and behavioral development, which may underpin elevated substance use during adolescence, are predispositions for or consequences of substance use initiation. Here, we examine behavioral and neuroimaging indices at early and mid-adolescence in drug-naive youths to identify possible predisposing factors for substance use initiation and its possible consequences. Method: Among 304 drug-naive adolescents at baseline (age 14 years) from the IMAGEN dataset, 83 stayed drug-naive, 133 used alcohol on 1 to 9 occasions, 42 on 10 to 19 occasions, 27 on 20 to 39 occasions, and 19 on >40 occasions at follow-up (age 16 years). Baseline measures included brain activation during the Monetary Incentive Delay task. Data at both baseline and follow-up included measures of trait impulsivity and delay discounting. Results: From baseline to follow-up, impulsivity decreased in the 0 and 1- to 9-occasions groups (p < .004), did not change in the 10- to 19-occasions and 20- to 29-occasions groups (p > .294), and uncharacteristically increased in the >40-occasions group (p = .046). Furthermore, blunted medial orbitofrontal cortex activation during reward outcome at baseline significantly predicted higher alcohol use frequency at follow-up, above and beyond behavioral and clinical variables (p = .008). Conclusion: These results suggest that the transition from no use to frequent drinking in early to mid-adolescence may disrupt normative developmental changes in behavioral control. In addition, blunted activity of the medial orbitofrontal cortex during reward outcome may underscore a predisposition toward the development of more severe alcohol use in adolescents. This distinction is clinically important, as it informs early intervention efforts in preventing the onset of substance use disorder in adolescents.
KW - adolescence
KW - alcohol use
KW - IMAGEN
KW - impulsivity
KW - reward processing
UR - http://www.scopus.com/inward/record.url?scp=85100676543&partnerID=8YFLogxK
U2 - 10.1016/j.jaac.2020.08.443
DO - 10.1016/j.jaac.2020.08.443
M3 - Article
C2 - 33011213
AN - SCOPUS:85100676543
SN - 0890-8567
VL - 60
SP - 623
EP - 636
JO - Journal of the American Academy of Child and Adolescent Psychiatry
JF - Journal of the American Academy of Child and Adolescent Psychiatry
IS - 5
ER -