A Developmental Perspective on Facets of Impulsivity and Brain Activity Correlates From Adolescence to Adulthood
Anna Kaiser, Nathalie Holz, Tobias Banaschewski, Sarah Baumeister, Arun L.W. Bokde, Sylvane Desrivières, Herta Flor, Juliane H. Fröhner, Antoine Grigis, Hugh Garavan, Penny Gowland, Andreas Heinz, Bernd Ittermann, Jean‐Luc Martinot, Marie‐Laure Paillère Martinot, Éric Artiges, Sabina Millenet, Dimitri Papadopoulos Orfanos, Luise Poustka, Emanuel Schwarz, Michael N. Smolka, Henrik Walter, Robert Whelan, Günter Schumann, Daniel Brandeis, Frauke Nees, Tobias Banaschewski, Gareth J. Barker, Arun L.W. Bokde, Sylvane Desrivières, Herta Flor, Antoine Grigis, Hugh Garavan, Penny Gowland, Andreas Heinz, Rüdiger Brühl, Jean‐Luc Martinot, Marie‐Laure Paillère Martinot, Éric Artiges, Frauke Nees, Dimitri Papadopoulos Orfanos, Hervé Lemaître, Tomáš Paus, Luise Poustka, Sarah Hohmann, Sabina Millenet, Juliane H. Fröhner, Lauren Robinson, Michael N. Smolka, Henrik Walter, Jeanne M. Winterer, Robert Whelan, Günter Schumann
Abstract
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.