NeuroImage (Apr 2020)
Sex effects on structural maturation of the limbic system and outcomes on emotional regulation during adolescence
- Pauline Bezivin Frere,
- Nora C. Vetter,
- Eric Artiges,
- Irina Filippi,
- Rubén Miranda,
- Hélène Vulser,
- Marie-Laure Paillère-Martinot,
- Veronika Ziesch,
- Patricia Conrod,
- Anna Cattrell,
- Henrik Walter,
- Jurgen Gallinat,
- Uli Bromberg,
- Sarah Jurk,
- Eva Menningen,
- Vincent Frouin,
- Dimitri Papadopoulos Orfanos,
- Argyris Stringaris,
- Jani Penttilä,
- Betteke van Noort,
- Yvonne Grimmer,
- Gunter Schumann,
- Michael N. Smolka,
- Jean-Luc Martinot,
- Hervé Lemaître
Affiliations
- Pauline Bezivin Frere
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France
- Nora C. Vetter
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Germany
- Eric Artiges
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France; Groupe Hospitalier Nord Essonne, Psychiatry Department 91G16, Orsay, France
- Irina Filippi
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France
- Rubén Miranda
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France; APHP, Department of Psychiatry and Addictology, Paul Brousse Hospital, Villejuif, France
- Hélène Vulser
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France
- Marie-Laure Paillère-Martinot
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France
- Veronika Ziesch
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Germany
- Patricia Conrod
- Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, United Kingdom; Department of Psychiatry, Université de Montreal, CHU Ste Justine Hospital, 175 Chemin de la Côte-Sainte-Catherine, Montréal, QC, H3T 1C4, Canada
- Anna Cattrell
- Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, United Kingdom
- Henrik Walter
- Charité Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
- Jurgen Gallinat
- University Medical Centre Hamburg-Eppendorf, Hamburg, Germany
- Uli Bromberg
- University Medical Centre Hamburg-Eppendorf, Hamburg, Germany
- Sarah Jurk
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Germany
- Eva Menningen
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Germany
- Vincent Frouin
- Neurospin, Commissariat à l’Energie Atomique, Université Paris-Saclay, Gif-sur-Yvette, Paris, France
- Dimitri Papadopoulos Orfanos
- Neurospin, Commissariat à l’Energie Atomique, Université Paris-Saclay, Gif-sur-Yvette, Paris, France
- Argyris Stringaris
- National Institute of Mental Health / NIH, 15K North Drive, Bethesda, MD, 20892, USA
- Jani Penttilä
- Department of Social and Health Care, Psychosocial Services Adolescent Outpatient Clinic Kauppakatu 14, Lahti, Finland
- Betteke van Noort
- Charité Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
- Yvonne Grimmer
- Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
- Gunter Schumann
- Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, United Kingdom; PONS Research Group, Dept of Psychiatry and Psychotherapy, Campus Charite Mitte, Humboldt University, Berlin and Leibniz Institute for Neurobiology, Magdeburg, Germany; PONS-Centre, Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, PR China
- Michael N. Smolka
- Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Germany
- Jean-Luc Martinot
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France; Centre de Neuro-Imagerie de Recherche (Cenir), Institut du Cerveau et de la Moëlle épinière (ICM), Pitié-Salpêtrière Hospital, Paris, France
- Hervé Lemaître
- Inserm, UMR 1000, Research Unit NeuroImaging and Psychiatry, Univ Paris Sud, Université Paris-Saclay, Université Paris Descartes, Digiteo Labs, Bâtiment 660, Gif-sur-Yvette, France; Corresponding author. Groupe d’Imagerie Neurofonctionnelle, Institut des Maladies Neurodégénératives, CNRS UMR 5293, Université de Bordeaux, Centre Broca Nouvelle-Aquitaine, 146 rue Léo Saignat - CS 61292 - Case 28 - Bordeaux cedex, France
- Journal volume & issue
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Vol. 210
p. 116441
Abstract
Though adolescence is a time of emerging sex differences in emotions, sex-related differences in the anatomy of the maturing brain has been under-explored over this period. The aim of this study was to investigate whether puberty and sexual differentiation in brain maturation could explain emotional differences between girls and boys during adolescence. We adapted a dedicated longitudinal pipeline to process structural and diffusion images from 335 typically developing adolescents between 14 and 16 years. We used voxel-based and Regions of Interest approaches to explore sex and puberty effects on brain and behavioral changes during adolescence. Sexual differences in brain maturation were characterized by amygdala and hippocampal volume increase in boys and decrease in girls. These changes were mediating the sexual differences in positive emotional regulation as illustrated by positive attributes increase in boys and decrease in girls. Moreover, the differential maturation rates between the limbic system and the prefrontal cortex highlighted the delayed maturation in boys compared to girls. This is the first study to show the sex effects on the differential cortico/subcortical maturation rates and the interaction between sex and puberty in the limbic system maturation related to positive attributes, reported as being protective from emotional disorders.
