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A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood

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...

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Autores principales: Kaiser, Anna, Holz, Nathalie E., Banaschewski, Tobias, Baumeister, Sarah, Bokde, Arun L.W., Desrivières, Sylvane, Flor, Herta, Fröhner, Juliane H., Grigis, Antoine, Garavan, Hugh, Gowland, Penny, Heinz, Andreas, Ittermann, Bernd, Martinot, Jean-Luc, Paillère Martinot, Marie-Laure, Artiges, Eric, Millenet, Sabina, Orfanos, Dimitri Papadopoulos, Poustka, Luise, Schwarz, Emanuel, Smolka, Michael N., Walter, Henrik, Whelan, Robert, Schumann, Gunter, Brandeis, Daniel, Nees, Frauke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier, Inc 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9636026/
https://www.ncbi.nlm.nih.gov/pubmed/35182817
http://dx.doi.org/10.1016/j.bpsc.2022.02.003
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author Kaiser, Anna
Holz, Nathalie E.
Banaschewski, Tobias
Baumeister, Sarah
Bokde, Arun L.W.
Desrivières, Sylvane
Flor, Herta
Fröhner, Juliane H.
Grigis, Antoine
Garavan, Hugh
Gowland, Penny
Heinz, Andreas
Ittermann, Bernd
Martinot, Jean-Luc
Paillère Martinot, Marie-Laure
Artiges, Eric
Millenet, Sabina
Orfanos, Dimitri Papadopoulos
Poustka, Luise
Schwarz, Emanuel
Smolka, Michael N.
Walter, Henrik
Whelan, Robert
Schumann, Gunter
Brandeis, Daniel
Nees, Frauke
author_facet Kaiser, Anna
Holz, Nathalie E.
Banaschewski, Tobias
Baumeister, Sarah
Bokde, Arun L.W.
Desrivières, Sylvane
Flor, Herta
Fröhner, Juliane H.
Grigis, Antoine
Garavan, Hugh
Gowland, Penny
Heinz, Andreas
Ittermann, Bernd
Martinot, Jean-Luc
Paillère Martinot, Marie-Laure
Artiges, Eric
Millenet, Sabina
Orfanos, Dimitri Papadopoulos
Poustka, Luise
Schwarz, Emanuel
Smolka, Michael N.
Walter, Henrik
Whelan, Robert
Schumann, Gunter
Brandeis, Daniel
Nees, Frauke
author_sort Kaiser, Anna
collection PubMed
description 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.
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spelling pubmed-96360262022-11-07 A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood Kaiser, Anna Holz, Nathalie E. Banaschewski, Tobias Baumeister, Sarah Bokde, Arun L.W. Desrivières, Sylvane Flor, Herta Fröhner, Juliane H. Grigis, Antoine Garavan, Hugh Gowland, Penny Heinz, Andreas Ittermann, Bernd Martinot, Jean-Luc Paillère Martinot, Marie-Laure Artiges, Eric Millenet, Sabina Orfanos, Dimitri Papadopoulos Poustka, Luise Schwarz, Emanuel Smolka, Michael N. Walter, Henrik Whelan, Robert Schumann, Gunter Brandeis, Daniel Nees, Frauke Biol Psychiatry Cogn Neurosci Neuroimaging Archival Report 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. Elsevier, Inc 2022-11 /pmc/articles/PMC9636026/ /pubmed/35182817 http://dx.doi.org/10.1016/j.bpsc.2022.02.003 Text en © 2022 Society of Biological Psychiatry. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Archival Report
Kaiser, Anna
Holz, Nathalie E.
Banaschewski, Tobias
Baumeister, Sarah
Bokde, Arun L.W.
Desrivières, Sylvane
Flor, Herta
Fröhner, Juliane H.
Grigis, Antoine
Garavan, Hugh
Gowland, Penny
Heinz, Andreas
Ittermann, Bernd
Martinot, Jean-Luc
Paillère Martinot, Marie-Laure
Artiges, Eric
Millenet, Sabina
Orfanos, Dimitri Papadopoulos
Poustka, Luise
Schwarz, Emanuel
Smolka, Michael N.
Walter, Henrik
Whelan, Robert
Schumann, Gunter
Brandeis, Daniel
Nees, Frauke
A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
title A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
title_full A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
title_fullStr A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
title_full_unstemmed A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
title_short A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
title_sort developmental perspective on facets of impulsivity and brain activity correlates from adolescence to adulthood
topic Archival Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9636026/
https://www.ncbi.nlm.nih.gov/pubmed/35182817
http://dx.doi.org/10.1016/j.bpsc.2022.02.003
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