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

Anna Kaiser; Nathalie E 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; Eric Artiges; Sabina Millenet; Dimitri Papadopoulos Orfanos; Luise Poustka; Emanuel Schwarz; Michael N Smolka; Henrik Walter; Robert Whelan; Gunter Schumann; Daniel Brandeis; Frauke Nees; IMAGEN Consortium

doi:10.1016/j.bpsc.2022.02.003

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

Biol Psychiatry Cogn Neurosci Neuroimaging. 2022 Nov;7(11):1103-1115. doi: 10.1016/j.bpsc.2022.02.003. Epub 2022 Feb 16.

Authors

Anna Kaiser¹, Nathalie E Holz², Tobias Banaschewski³, Sarah Baumeister³, Arun L W Bokde⁴, Sylvane Desrivières⁵, Herta Flor⁶, Juliane H Fröhner⁷, Antoine Grigis⁸, Hugh Garavan⁹, Penny Gowland¹⁰, Andreas Heinz¹¹, Bernd Ittermann¹², Jean-Luc Martinot¹³, Marie-Laure Paillère Martinot¹⁴, Eric Artiges¹⁵, Sabina Millenet³, Dimitri Papadopoulos Orfanos⁸, Luise Poustka¹⁶, Emanuel Schwarz¹⁷, Michael N Smolka⁷, Henrik Walter¹⁸, Robert Whelan¹⁹, Gunter Schumann²⁰, Daniel Brandeis²¹, Frauke Nees²²; IMAGEN Consortium

Affiliations

¹ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany. Electronic address: anna.kaiser@zi-mannheim.de.
² Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, the Netherlands; Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, the Netherlands.
³ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁴ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
⁵ Centre for Population Neuroscience and Precision Medicine, Institute of Psychiatry, Psychology & Neuroscience, Social, Genetic and Developmental Psychiatry Centre, King's College London, London, United Kingdom.
⁶ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany.
⁷ Department of Psychiatry and Neuroimaging Center, Technical University Dresden, Dresden, Germany.
⁸ NeuroSpin, Commissariat à l'énergie atomique, Université Paris-Saclay, Gif-sur-Yvette, France.
⁹ Department of Psychology, University of Vermont, Burlington, Vermont.
¹⁰ Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom.
¹¹ Department of Psychiatry and Psychotherapy, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
¹² Physikalisch-Technische Bundesanstalt, Braunschweig and Berlin, Germany.
¹³ Institut National de la Santé et de la Recherche Médicale, Institut National de la Santé et de la Recherche Médicale U A10 "Trajectoires développementales en psychiatrie", Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, Centre National de la Recherche Scientifique, Centre Borelli, Gif-sur-Yvette, France.
¹⁴ Institut National de la Santé et de la Recherche Médicale, Institut National de la Santé et de la Recherche Médicale U A10 "Trajectoires développementales en psychiatrie", Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, Centre National de la Recherche Scientifique, Centre Borelli, Gif-sur-Yvette, France; Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, L'Assistance Publique-Hôpitaux de Paris Sorbonne Université, Paris, France.
¹⁵ Institut National de la Santé et de la Recherche Médicale, Institut National de la Santé et de la Recherche Médicale U A10 "Trajectoires développementales en psychiatrie", Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, Centre National de la Recherche Scientifique, Centre Borelli, Gif-sur-Yvette, France; Psychiatry Department 91G16, Orsay Hospital, Orsay, France.
¹⁶ Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, Göttingen, Germany.
¹⁷ Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹⁸ Department of Psychiatry and Psychotherapy, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Department of Psychiatry, University of Vermont, Burlington, Vermont.
¹⁹ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
²⁰ Population Neuroscience Research Group, Department of Psychiatry and Psychotherapy, Campus Charite Mitte, Humboldt University, Berlin, Germany; Leibniz Institute for Neurobiology, Magdeburg, Germany; Centre for Population Neuroscience and Precision Medicine, Institute of Psychiatry, Psychology & Neuroscience, Social, Genetic and Developmental Psychiatry Centre, King's College London, London, United Kingdom; Institute for Science and Technology of Brain-inspired Intelligence, Fudan University, Shanghai, China.
²¹ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry, University of Zürich, Zürich, Switzerland; Neuroscience Center Zürich, Swiss Federal Institute of Technology and University of Zürich, Zürich, Switzerland.
²² Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany.

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.

Keywords: Biomarker; Developmental trajectories; Impulsivity; Inhibitory control; Prediction; Reward anticipation.

Publication types

Multicenter Study
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Adult
Cohort Studies
Humans
Impulsive Behavior* / physiology
Magnetic Resonance Imaging
Reward
Ventral Striatum*
Young Adult

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

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