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Differential associations of adolescent versus young adult cannabis initiation with longitudinal brain change and behavior

Molecular Psychiatry volume 28, pages 5173–5182 (2023)Cite this article

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Abstract

Leveraging ~10 years of prospective longitudinal data on 704 participants, we examined the effects of adolescent versus young adult cannabis initiation on MRI-assessed cortical thickness development and behavior. Data were obtained from the IMAGEN study conducted across eight European sites. We identified IMAGEN participants who reported being cannabis-naïve at baseline and had data available at baseline, 5-year, and 9-year follow-up visits. Cannabis use was assessed with the European School Survey Project on Alcohol and Drugs. T1-weighted MR images were processed through the CIVET pipeline. Cannabis initiation occurring during adolescence (14–19 years) and young adulthood (19–22 years) was associated with differing patterns of longitudinal cortical thickness change. Associations between adolescent cannabis initiation and cortical thickness change were observed primarily in dorso- and ventrolateral portions of the prefrontal cortex. In contrast, cannabis initiation occurring between 19 and 22 years of age was associated with thickness change in temporal and cortical midline areas. Follow-up analysis revealed that longitudinal brain change related to adolescent initiation persisted into young adulthood and partially mediated the association between adolescent cannabis use and past-month cocaine, ecstasy, and cannabis use at age 22. Extent of cannabis initiation during young adulthood (from 19 to 22 years) had an indirect effect on psychotic symptoms at age 22 through thickness change in temporal areas. Results suggest that developmental timing of cannabis exposure may have a marked effect on neuroanatomical correlates of cannabis use as well as associated behavioral sequelae. Critically, this work provides a foundation for neurodevelopmentally informed models of cannabis exposure in humans.

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Fig. 1: Adolescent cannabis use and cortical thickness in young adulthood.
Fig. 2: Longitudinal linear mixed-effects model results for group-level analysis.
Fig. 3: Cortical thickness trajectories from 14 to 22 years of age.
Fig. 4: Cannabis use and cortical thickness in young adulthood (19–22).
Fig. 5: Cannabis and age-related cortical thickness change.

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Acknowledgements

This work received support from the following sources: the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behavior 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; Forschungsnetz IMAC-Mind 01GL1745B), 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), 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; R01 MH085772-01A1), and by NIH Consortium grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence. 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. Dr Albaugh is supported by K08 MH121654-01A1 and a NARSAD Young Investigator Grant from the Brain & Behavior Research Foundation. Drs Albaugh and Garavan had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the paper; and decision to submit the paper for publication.

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Authors and Affiliations

  1. Department of Psychiatry, University of Vermont, Burlington, VT, USA

    Matthew D. Albaugh, Max M. Owens, Anthony Juliano, Jonatan Ottino-Gonzalez, Renata Cupertino, Zhipeng Cao, Scott Mackey, Alexandra Potter & Hugh Garavan

  2. McConnell Brain Imaging Centre, McGill University, Montreal, QC, Canada

    Claude Lepage, Pierre Rioux & Alan Evans

  3. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany

    Tobias Banaschewski, Frauke Nees & Sabina Millenet

  4. Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland

    Arun L. W. Bokde

  5. Department of Psychiatry, University of Montreal, Montreal, QC, Canada

    Patricia Conrod

  6. Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, London, UK

    Sylvane Desrivières & Gunter Schumann

  7. Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany

    Herta Flor & Frauke Nees

  8. Department of Psychology, School of Social Sciences, University of Mannheim, 68131, Mannheim, Germany

    Herta Flor

  9. NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France

    Antoine Grigis & Dimitri Papadopoulos Orfanos

  10. Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom

    Penny Gowland

  11. Department of Psychiatry and Psychotherapy CCM, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany

    Andreas Heinz & Henrik Walter

  12. Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Berlin, Germany

    Bernd Ittermann

  13. Institut National de la Santé et de la Recherche Médicale, INSERM U A10 “Trajectoires développementales en psychiatrie”, Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France

    Jean-Luc Martinot

  14. Institut National de la Santé et de la Recherche Médicale, INSERM U A10 “Trajectoires développementales en psychiatrie”; Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli; and AP-HP.Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France

    Marie-Laure Paillère Martinot

  15. Institut National de la Santé et de la Recherche Médicale, INSERM U1299 “Developmental trajectories & psychiatry””; Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli; Gif-sur-Yvette; and Etablissement Public de Santé (EPS) Barthélemy Durand, 91700, Sainte-Geneviève-des-Bois, France

    Eric Artiges

  16. Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany

    Frauke Nees

  17. Departments of Psychiatry and Neuroscience, Faculty of Medicine and Centre Hospitaliere Universitaire Sainte-Justine, University of Montreal, Montreal, QC, H3T 1C5, Canada

    Tomáš Paus

  18. Departments of Psychology and Psychiatry, University of Toronto, Toronto, ON, M6A 2E1, Canada

    Tomáš Paus

  19. Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany

    Luise Poustka

  20. Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany

    Juliane H. Fröhner & Michael N. Smolka

  21. School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland

    Robert Whelan

  22. PONS Research Group, Dept of Psychiatry and Psychotherapy, Campus Charite Mitte, Humboldt University, Berlin and Leibniz Institute for Neurobiology, Magdeburg, Germany

    Gunter Schumann

  23. Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, P. R. China

    Gunter Schumann

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  1. Matthew D. Albaugh
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Consortia

IMAGEN Consortium

  • Tobias Banaschewski
  • , Arun L. W. Bokde
  • , Sylvane Desrivières
  • , Herta Flor
  • , Antoine Grigis
  • , Penny Gowland
  • , Andreas Heinz
  • , Bernd Ittermann
  • , Jean-Luc Martinot
  • , Marie-Laure Paillère Martinot
  • , Eric Artiges
  • , Frauke Nees
  • , Dimitri Papadopoulos Orfanos
  • , Tomáš Paus
  • , Luise Poustka
  • , Sabina Millenet
  • , Juliane H. Fröhner
  • , Michael N. Smolka
  • , Henrik Walter
  • , Robert Whelan
  • , Gunter Schumann
  •  & Hugh Garavan

Contributions

MA conceived and performed the analysis, interpreted the results, and wrote the paper. AP and HG supervised the project, interpreted the results, and edited the paper. CL and PR assisted in the storage and processing of neuroimaging data. The rest of the authors contributed to the data acquisition and sharing and edited the paper.

Corresponding author

Correspondence to Matthew D. Albaugh.

Ethics declarations

Competing interests

Dr TB has served as an advisor or consultant to Bristol-Myers Squibb, Desitin Arzneimittel, Eli Lilly, Medice, Novartis, Pfizer, Shire, UCB, and Vifor Pharma; he has received conference attendance support, conference support, or speaking fees from Eli Lilly, Janssen McNeil, Medice, Novartis, Shire, and UCB; and he is involved in clinical trials conducted by Eli Lilly, Novartis, and Shire; the present work is unrelated to these relationships. The other authors report no biomedical financial interests or potential competing interests.

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Albaugh, M.D., Owens, M.M., Juliano, A. et al. Differential associations of adolescent versus young adult cannabis initiation with longitudinal brain change and behavior. Mol Psychiatry 28, 5173–5182 (2023). https://doi.org/10.1038/s41380-023-02148-2

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  • DOI: https://doi.org/10.1038/s41380-023-02148-2

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