Abstract

This study examines the effects of puberty and sex on the intrinsic functional connectivity (iFC) of brain networks, with a focus on the default-mode network (DMN). Consistently implicated in depressive disorders, the DMN’s function may interact with puberty and sex in the development of these disorders, whose onsets peak in adolescence, and which show strong sex disproportionality (females > males). The main question concerns how the DMN evolves with puberty as a function of sex. These effects are expected to involve within- and between-network iFC, particularly, the salience and the central-executive networks, consistent with the Triple-Network Model. Resting-state scans of an adolescent community sample (n = 304, male/female: 157/147; mean/std age: 14.6/0.41 years), from the IMAGEN database, were analyzed using the AFNI software suite and a data reduction strategy for the effects of puberty and sex. Three midline regions (medial prefrontal, pregenual anterior cingulate, and posterior cingulate), within the DMN and consistently implicated in mood disorders, were selected as seeds. Within- and between-network clusters of the DMN iFC changed with pubertal maturation differently in boys and girls (puberty-X-sex). Specifically, pubertal maturation predicted weaker iFC in girls and stronger iFC in boys. Finally, iFC was stronger in boys than girls independently of puberty. Brain–behavior associations indicated that lower connectivity of the anterior cingulate seed predicted higher internalizing symptoms at 2-year follow-up. In conclusion, weaker iFC of the anterior DMN may signal disconnections among circuits supporting mood regulation, conferring risk for internalizing disorders.

Details

Title
Pubertal maturation and sex effects on the default-mode network connectivity implicated in mood dysregulation
Author
Ernst, Monique 1 ; Benson, Brenda 1 ; Artiges Eric 2 ; Gorka, Adam X 1 ; Lemaitre Herve 3   VIAFID ORCID Logo  ; Lago, Tiffany 1 ; Miranda, Ruben 4 ; Banaschewski Tobias 5 ; Bokde Arun L W 6 ; Bromberg Uli 7 ; Brühl Rüdiger 8 ; Büchel, Christian 7 ; Cattrell Anna 9 ; Conrod, Patricia 10 ; Sylvane, Desrivières 9   VIAFID ORCID Logo  ; Fadai Tahmine 7 ; Flor Herta 11 ; Grigis Antoine 12 ; Gallinat Juergen 13 ; Garavan Hugh 14 ; Gowland, Penny 15 ; Grimmer, Yvonne 5 ; Heinz, Andreas 16 ; Kappel Viola 17 ; Nees Frauke 11 ; Papadopoulos-Orfanos Dimitri 12   VIAFID ORCID Logo  ; Penttilä Jani 18 ; Poustka Luise 19 ; Smolka, Michael N 20   VIAFID ORCID Logo  ; Stringaris Argyris 21 ; Struve Maren 22 ; van Noort Betteke M 17 ; Walter, Henrik 16   VIAFID ORCID Logo  ; Whelan, Robert 22 ; Schumann Gunter 9 ; Grillon, Christian 1 ; Paillère, Martinot Marie-Laure 23 ; Martinot Jean-Luc 24 ; Dalley, J; Subramaniam, N; Theobald, D; Bach, C; Barker, G J; Fauth-Bühler, M; Millenet, S; Spanagel, R; Albrecht, L; Ivanov, N; Rapp, M; Reuter, J; Strache, N; Ströhle, A; Poline, J B; Schwartz, Y; Thyreau, B; Ireland, J; Rogers, J; Bordas, N; Bricaud, Z; Filippi, I; Galinowski, A; Gollier-Briant, F; Hall, D; Havatzias, S; Jia, T; Mallik, C; Nymberg, C; Ruggeri, B; Smith, L; Stueber, K; Topper, L; Werts, H; Brühl, R R; Ihlenfeld, A; Walaszek, B; Hübner, T; Müller, K; Paus, T; Ripke, S; Mennigen, E; Schmidt, D; Vetter, N C; Ziesch, V; Carter, D; Connolly, C; Nugent, S; Jones, J; Yacubian, J; Schneider, S; Head, K; Heym, N; Newman, C; Pausova, Z; Tahmasebi, A; Stephens, D

1  NIMH/NIH, Bethesda, USA (GRID:grid.416868.5) (ISNI:0000 0004 0464 0574) 
2  University Paris-Saclay, and University Paris Descartes, INSERM, UMR 1000, Research unit “Neuroimaging and Psychiatry”, DIGITEO Labs, Gif sur Yvette, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914); University Paris-Saclay, DIGITEO Labs, INSERM, UMR 1000, Faculté de médecine, Gif sur Yvette, France (GRID:grid.460789.4) (ISNI:0000 0004 4910 6535); University Paris Descartes, Paris, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914); Brain & Spine Institute, Center for Neuroimaging Research (CENIR), Paris, France (GRID:grid.411439.a) (ISNI:0000 0001 2150 9058); Psychiatry Department 91G16, Orsay Hospital, Paris, France (GRID:grid.411439.a) 
3  University Paris-Saclay, and University Paris Descartes, INSERM, UMR 1000, Research unit “Neuroimaging and Psychiatry”, DIGITEO Labs, Gif sur Yvette, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914); University Paris-Saclay, DIGITEO Labs, INSERM, UMR 1000, Faculté de médecine, Gif sur Yvette, France (GRID:grid.460789.4) (ISNI:0000 0004 4910 6535) 
4  University Paris-Saclay, and University Paris Descartes, INSERM, UMR 1000, Research unit “Neuroimaging and Psychiatry”, DIGITEO Labs, Gif sur Yvette, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914) 
5  Heidelberg University, Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Mannheim, Germany (GRID:grid.7700.0) (ISNI:0000 0001 2190 4373) 
6  Trinity College, Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neurosciences, Dublin, Ireland (GRID:grid.8217.c) (ISNI:0000 0004 1936 9705) 
7  University Medical Centre Hamburg-Eppendorf, Hamburg, Germany (GRID:grid.13648.38) (ISNI:0000 0001 2180 3484) 
8  Physikalisch-Technische Bundesanstalt, Berlin, Germany (GRID:grid.4764.1) (ISNI:0000 0001 2186 1887) 
9  King’s College London, Medical Research Council - Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology & Neuroscience, London, United Kingdom (GRID:grid.13097.3c) (ISNI:0000 0001 2322 6764) 
10  King’s College London, Department of Psychological Medicine and Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, London, United Kingdom (GRID:grid.13097.3c) (ISNI:0000 0001 2322 6764); Université de Montréal, CHU Ste Justine Hospital, Department of Psychiatry, Montréal, Canada (GRID:grid.14848.31) (ISNI:0000 0001 2292 3357) 
11  Heidelberg University, Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Mannheim, Germany (GRID:grid.7700.0) (ISNI:0000 0001 2190 4373); University of Mannheim, Department of Psychology, School of Social Sciences, Mannheim, Germany (GRID:grid.5601.2) (ISNI:0000 0001 0943 599X) 
12  Neurospin, Commissariat à l’Energie Atomique, CEA-Saclay Center, Saclay, France (GRID:grid.5601.2) 
13  University Medical Center Hamburg-Eppendorf, Department of Psychiatry and Psychotherapy, Hamburg, Germany (GRID:grid.13648.38) (ISNI:0000 0001 2180 3484) 
14  University of Vermont, Departments of Psychiatry and Psychology, Burlington, USA (GRID:grid.59062.38) (ISNI:0000 0004 1936 7689) 
15  University Park, Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom (GRID:grid.4563.4) (ISNI:0000 0004 1936 8868) 
16  Charité-Universitätsmedizin Berlin, Department of Psychiatry and Psychotherapy, Campus CharitéMitte, Berlin, Germany (GRID:grid.6363.0) (ISNI:0000 0001 2218 4662) 
17  Charité-Universitätsmedizin Berlin, Department of Child and Adolescent Psychiatry Psychosomatics and Psychotherapy, Campus CharitéMitte, Berlin, Germany (GRID:grid.6363.0) (ISNI:0000 0001 2218 4662) 
18  University of Tampere, Department of Social and Health Care, Psychosocial Services Adolescent Outpatient Clinic, Lahti, Finland (GRID:grid.502801.e) (ISNI:0000 0001 2314 6254) 
19  Heidelberg University, Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Mannheim, Germany (GRID:grid.7700.0) (ISNI:0000 0001 2190 4373); Medical University of Vienna, Department of Child and Adolescent Psychiatry and Psychotherapy, Vienna, Austria (GRID:grid.22937.3d) (ISNI:0000 0000 9259 8492) 
20  Technische Universität Dresden, Department of Psychiatry and Neuroimaging Center, Dresden, Germany (GRID:grid.4488.0) (ISNI:0000 0001 2111 7257) 
21  NIMH/NIH, Bethesda, USA (GRID:grid.416868.5) (ISNI:0000 0004 0464 0574); King’s College London, Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, London, United Kingdom (GRID:grid.13097.3c) (ISNI:0000 0001 2322 6764) 
22  University College, Department of Psychology, Dublin, Ireland (GRID:grid.7886.1) (ISNI:0000 0001 0768 2743) 
23  University Paris-Saclay, and University Paris Descartes, INSERM, UMR 1000, Research unit “Neuroimaging and Psychiatry”, DIGITEO Labs, Gif sur Yvette, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914); University Paris Descartes, Paris, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914); Pitié-Salpêtrière Hospital, AP-HP, Department of Child and Adolescent Psychiatry, Paris, France (GRID:grid.411439.a) (ISNI:0000 0001 2150 9058); Sorbonne Universités, Paris, France (GRID:grid.462844.8) (ISNI:0000 0001 2308 1657) 
24  University Paris-Saclay, and University Paris Descartes, INSERM, UMR 1000, Research unit “Neuroimaging and Psychiatry”, DIGITEO Labs, Gif sur Yvette, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914); University Paris-Saclay, DIGITEO Labs, INSERM, UMR 1000, Faculté de médecine, Gif sur Yvette, France (GRID:grid.460789.4) (ISNI:0000 0004 4910 6535); University Paris Descartes, Paris, France (GRID:grid.10992.33) (ISNI:0000 0001 2188 0914); Brain & Spine Institute, Center for Neuroimaging Research (CENIR), Paris, France (GRID:grid.411439.a) (ISNI:0000 0001 2150 9058) 
Publication year
2019
Publication date
Dec 2019
Publisher
Nature Publishing Group
e-ISSN
21583188
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.1038/s41398-019-0433-6
ProQuest document ID
2185863240
Copyright
This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.