TY - JOUR
T1 - A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
AU - IMAGEN Consortium
AU - Kaiser, Anna
AU - Holz, Nathalie E.
AU - Banaschewski, Tobias
AU - Baumeister, Sarah
AU - Bokde, Arun L.W.
AU - Desrivières, Sylvane
AU - Flor, Herta
AU - Fröhner, Juliane H.
AU - Grigis, Antoine
AU - Garavan, Hugh
AU - Gowland, Penny
AU - Heinz, Andreas
AU - Ittermann, Bernd
AU - Martinot, Jean Luc
AU - Paillère Martinot, Marie Laure
AU - Artiges, Eric
AU - Millenet, Sabina
AU - Orfanos, Dimitri Papadopoulos
AU - Poustka, Luise
AU - Schwarz, Emanuel
AU - Smolka, Michael N.
AU - Walter, Henrik
AU - Whelan, Robert
AU - Schumann, Gunter
AU - Brandeis, Daniel
AU - Nees, Frauke
AU - Barker, Gareth J.
AU - Brühl, Rüdiger
AU - Lemaitre, Herve
AU - Paus, Tomáš
AU - Hohmann, Sarah
AU - Robinson, Lauren
AU - Winterer, Jeanne M.
N1 - Funding Information:
This work was supported by the research consortium on ADHD, ESCA-Life, funded by the German Federal Ministry of Education and Research (Grant No. FKZ 01EE1408E [to TB]), European Union–funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (Grant No. LSHM-CT-2007-037286), Horizon 2020–funded European Research Council Advanced Grant STRATIFY (Brain network based stratification of reinforcement-related disorders) (Grant No. 695313 ), Human Brain Project (Grant Nos. HBP SGA 2, 785907 , and HBP SGA 3, 945539 ), Medical Research Council Grant c-VEDA (Consortium on Vulnerability to Externalizing Disorders and Addictions) (Grant No. MR/N000390/1 ), National Institutes of Health (NIH) (A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers) (Grant No. R01DA049238 ), National Institute for Health Research Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, Bundesministerium für Bildung und Forschung (Grant Nos. 01GS08152, 01EV0711, and Forschungsnetz AERIAL 01EE1406A and 01EE1406B), Deutsche Forschungsgemeinschaft (Grant Nos. SM 80/7-2 , SFB 940 , TRR 265 , and NE 1383/14-1 ), Medical Research Foundation and Medical Research Council (Grant Nos. MR/R00465X/1 and MR/S020306/1 ), NIH-funded ENIGMA (Grant Nos. 5U54EB020403-05 and 1R56AG058854-01 ), Agence Nationale de la Recherche (Grant Nos. ANR-12-SAMA-0004 and AAPG2019—GeBra ), Eranet Neuron (Grant Nos. AF12-NEUR0008-01—WM2NA and ANR-18-NEUR00002-01—ADORe ), Fondation de France (Grant No. 00081242 ), Fondation pour la Recherche Médicale (Grant No. DPA20140629802 ), Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives, Assistance-Publique-Hôpitaux-de-Paris and Institut National de la Santé et de la Recherche Médicale (interface grant), Paris Sud University IDEX 2012, Fondation de l’Avenir (Grant No. AP-RM-17-013), Fédération pour la Recherche sur le Cerveau, NIH, Science Foundation Ireland (Grant No. 16/ERCD/3797 ), USA (Axon, Testosterone and Mental Health during Adolescence) (Grant No. RO1 MH085772-01A1), and NIH Consortium (Grant No. U54 EB020403), supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence.
Funding Information:
This work was supported by the research consortium on ADHD, ESCA-Life, funded by the German Federal Ministry of Education and Research (Grant No. FKZ 01EE1408E [to TB]), European Union–funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (Grant No. LSHM-CT-2007-037286), Horizon 2020–funded European Research Council Advanced Grant STRATIFY (Brain network based stratification of reinforcement-related disorders) (Grant No. 695313), Human Brain Project (Grant Nos. HBP SGA 2, 785907, and HBP SGA 3, 945539), Medical Research Council Grant c-VEDA (Consortium on Vulnerability to Externalizing Disorders and Addictions) (Grant No. MR/N000390/1), National Institutes of Health (NIH) (A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers) (Grant No. R01DA049238), National Institute for Health Research Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London, Bundesministerium für Bildung und Forschung (Grant Nos. 01GS08152, 01EV0711, and Forschungsnetz AERIAL 01EE1406A and 01EE1406B), Deutsche Forschungsgemeinschaft (Grant Nos. SM 80/7-2, SFB 940, TRR 265, and NE 1383/14-1), Medical Research Foundation and Medical Research Council (Grant Nos. MR/R00465X/1 and MR/S020306/1), NIH-funded ENIGMA (Grant Nos. 5U54EB020403-05 and 1R56AG058854-01), Agence Nationale de la Recherche (Grant Nos. ANR-12-SAMA-0004 and AAPG2019—GeBra), Eranet Neuron (Grant Nos. AF12-NEUR0008-01—WM2NA and ANR-18-NEUR00002-01—ADORe), Fondation de France (Grant No. 00081242), Fondation pour la Recherche Médicale (Grant No. DPA20140629802), Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives, Assistance-Publique-Hôpitaux-de-Paris and Institut National de la Santé et de la Recherche Médicale (interface grant), Paris Sud University IDEX 2012, Fondation de l'Avenir (Grant No. AP-RM-17-013), Fédération pour la Recherche sur le Cerveau, NIH, Science Foundation Ireland (Grant No. 16/ERCD/3797), USA (Axon, Testosterone and Mental Health during Adolescence) (Grant No. RO1 MH085772-01A1), and NIH Consortium (Grant No. U54 EB020403), supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence. The study data have been published online (September 17 2021) as part of AK's dissertation thesis (https://doi.org/10.11588/heidok.00030332). TB served in an advisory or consultancy role for ADHS Digital, InfectoPharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda; received conference support or speaker's fee from Medice and Takeda; and received royalties from Hogrefe, Kohlhammer, CIP Medien, and Oxford University Press. Gareth J. Barker has received honoraria from GE Healthcare for teaching on scanner programming courses. DB serves as an unpaid scientific consultant for a European Union–funded neurofeedback trial. LP served in an advisory or consultancy role for Roche and Vifor Pharma; received speaker's fee from Shire; and received royalties from Hogrefe, Kohlhammer, and Schattauer. The present work is unrelated to the above grants and relationships. All other authors report no biomedical financial interests or potential conflicts of interest.
Publisher Copyright:
© 2022 Society of Biological Psychiatry
PY - 2022/11
Y1 - 2022/11
N2 - Background: On a theoretical level, impulsivity represents a multidimensional construct associated with acting without foresight, inefficient inhibitory response control, and alterations in reward processing. On an empirical level, relationships and changes in associations between different measures of impulsivity from adolescence into young adulthood and their relation to neural activity during inhibitory control and reward anticipation have not been fully understood. Methods: We used data from IMAGEN, a longitudinal multicenter, population-based cohort study in which 2034 healthy adolescents were investigated at age 14, and 1383 were reassessed as young adults at age 19. We measured the construct of trait impulsivity using self-report questionnaires and neurocognitive indices of decisional impulsivity. With functional magnetic resonance imaging, we assessed brain activity during inhibition error processing using the stop signal task and during reward anticipation in the monetary incentive delay task. Correlations were analyzed, and mixed-effect models were fitted to explore developmental and predictive effects. Results: All self-report and neurocognitive measures of impulsivity proved to be correlated during adolescence and young adulthood. Further, pre-supplementary motor area and inferior frontal gyrus activity during inhibition error processing was associated with trait impulsivity in adolescence, whereas in young adulthood, a trend-level association with reward anticipation activity in the ventral striatum was found. For adult delay discounting, a trend-level predictive effect of adolescent neural activity during inhibition error processing emerged. Conclusions: Our findings help to inform theories of impulsivity about the development of its multidimensional nature and associated brain activity patterns and highlight the need for taking functional brain development into account when evaluating neuromarker candidates.
AB - Background: On a theoretical level, impulsivity represents a multidimensional construct associated with acting without foresight, inefficient inhibitory response control, and alterations in reward processing. On an empirical level, relationships and changes in associations between different measures of impulsivity from adolescence into young adulthood and their relation to neural activity during inhibitory control and reward anticipation have not been fully understood. Methods: We used data from IMAGEN, a longitudinal multicenter, population-based cohort study in which 2034 healthy adolescents were investigated at age 14, and 1383 were reassessed as young adults at age 19. We measured the construct of trait impulsivity using self-report questionnaires and neurocognitive indices of decisional impulsivity. With functional magnetic resonance imaging, we assessed brain activity during inhibition error processing using the stop signal task and during reward anticipation in the monetary incentive delay task. Correlations were analyzed, and mixed-effect models were fitted to explore developmental and predictive effects. Results: All self-report and neurocognitive measures of impulsivity proved to be correlated during adolescence and young adulthood. Further, pre-supplementary motor area and inferior frontal gyrus activity during inhibition error processing was associated with trait impulsivity in adolescence, whereas in young adulthood, a trend-level association with reward anticipation activity in the ventral striatum was found. For adult delay discounting, a trend-level predictive effect of adolescent neural activity during inhibition error processing emerged. Conclusions: Our findings help to inform theories of impulsivity about the development of its multidimensional nature and associated brain activity patterns and highlight the need for taking functional brain development into account when evaluating neuromarker candidates.
KW - Biomarker
KW - Developmental trajectories
KW - Impulsivity
KW - Inhibitory control
KW - Prediction
KW - Reward anticipation
UR - http://www.scopus.com/inward/record.url?scp=85129043424&partnerID=8YFLogxK
U2 - 10.1016/j.bpsc.2022.02.003
DO - 10.1016/j.bpsc.2022.02.003
M3 - Article
C2 - 35182817
AN - SCOPUS:85129043424
SN - 2451-9022
VL - 7
SP - 1103
EP - 1115
JO - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
JF - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
IS - 11
ER -