Abstract

Human cortical maturation has been posited to be organized along the sensorimotor-association axis, a hierarchical axis of brain organization that spans from unimodal sensorimotor cortices to transmodal association cortices. Here, we investigate the hypothesis that the development of functional connectivity during childhood through adolescence conforms to the cortical hierarchy defined by the sensorimotor-association axis. We tested this pre-registered hypothesis in four large-scale, independent datasets (total n = 3355; ages 5–23 years): the Philadelphia Neurodevelopmental Cohort (n = 1207), Nathan Kline Institute-Rockland Sample (n = 397), Human Connectome Project: Development (n = 625), and Healthy Brain Network (n = 1126). Across datasets, the development of functional connectivity systematically varied along the sensorimotor-association axis. Connectivity in sensorimotor regions increased, whereas connectivity in association cortices declined, refining and reinforcing the cortical hierarchy. These consistent and generalizable results establish that the sensorimotor-association axis of cortical organization encodes the dominant pattern of functional connectivity development.

Human cortical maturation is organized along the sensorimotor-association axis. Here, the authors investigate in multiple cohorts if the development of functional connectivity during adolescence conforms to this hierarchy.

Details

Title
Functional connectivity development along the sensorimotor-association axis enhances the cortical hierarchy
Author
Luo, Audrey C. 1   VIAFID ORCID Logo  ; Sydnor, Valerie J. 1   VIAFID ORCID Logo  ; Pines, Adam 2 ; Larsen, Bart 3   VIAFID ORCID Logo  ; Alexander-Bloch, Aaron F. 4   VIAFID ORCID Logo  ; Cieslak, Matthew 1   VIAFID ORCID Logo  ; Covitz, Sydney 1 ; Chen, Andrew A. 5 ; Esper, Nathalia Bianchini 6   VIAFID ORCID Logo  ; Feczko, Eric 6   VIAFID ORCID Logo  ; Franco, Alexandre R. 7 ; Gur, Raquel E. 4 ; Gur, Ruben C. 8   VIAFID ORCID Logo  ; Houghton, Audrey 9   VIAFID ORCID Logo  ; Hu, Fengling 10 ; Keller, Arielle S. 1 ; Kiar, Gregory 6   VIAFID ORCID Logo  ; Mehta, Kahini 1 ; Salum, Giovanni A. 11 ; Tapera, Tinashe 12 ; Xu, Ting 6   VIAFID ORCID Logo  ; Zhao, Chenying 13   VIAFID ORCID Logo  ; Salo, Taylor 1 ; Fair, Damien A. 14   VIAFID ORCID Logo  ; Shinohara, Russell T. 15 ; Milham, Michael P. 16   VIAFID ORCID Logo  ; Satterthwaite, Theodore D. 17   VIAFID ORCID Logo 

1  University of Pennsylvania, Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972) 
2  University of Pennsylvania, Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); Stanford University, Department of Psychiatry and Behavioral Sciences, Stanford, USA (GRID:grid.168010.e) (ISNI:0000 0004 1936 8956) 
3  University of Pennsylvania, Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Minnesota, Masonic Institute for the Developing Brain, Minneapolis, USA (GRID:grid.17635.36) (ISNI:0000 0004 1936 8657); University of Minnesota Medical School, Department of Pediatrics, Minneapolis, USA (GRID:grid.17635.36) (ISNI:0000000419368657) 
4  University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); Children’s Hospital of Philadelphia, Department of Child and Adolescent Psychiatry and Behavioral Science, Philadelphia, USA (GRID:grid.239552.a) (ISNI:0000 0001 0680 8770) 
5  Medical University of South Carolina, Division of Biostatistics and Bioinformatics, Department of Public Health Sciences, Charleston, USA (GRID:grid.259828.c) (ISNI:0000 0001 2189 3475) 
6  Child Mind Institute, Center for the Developing Brain, New York, USA (GRID:grid.428122.f) (ISNI:0000 0004 7592 9033) 
7  Child Mind Institute, Center for the Developing Brain, New York, USA (GRID:grid.428122.f) (ISNI:0000 0004 7592 9033); Nathan Kline Institute for Psychiatric Research, Center for Biomedical Imaging and Neuromodulation, Orangeburg, USA (GRID:grid.250263.0) (ISNI:0000 0001 2189 4777); NYU Grossman School of Medicine, Department of Psychiatry, New York, USA (GRID:grid.137628.9) (ISNI:0000 0004 1936 8753) 
8  University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972) 
9  University of Minnesota, Masonic Institute for the Developing Brain, Minneapolis, USA (GRID:grid.17635.36) (ISNI:0000 0004 1936 8657) 
10  University of Pennsylvania, Penn Statistics in Imaging and Visualization Center, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972) 
11  Child Mind Institute, Center for the Developing Brain, New York, USA (GRID:grid.428122.f) (ISNI:0000 0004 7592 9033); Universidade Federal do Rio Grande do Sul, Section on Negative Affect and Social Processes, Hospital de Clínicas de Porto Alegre, Porto Alegre, Brazil (GRID:grid.8532.c) (ISNI:0000 0001 2200 7498) 
12  University of Pennsylvania, Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); Northeastern University, Khoury College of Computer Sciences, Boston, USA (GRID:grid.261112.7) (ISNI:0000 0001 2173 3359) 
13  University of Pennsylvania, Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Bioengineering, School of Engineering and Applied Science, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972) 
14  University of Minnesota, Masonic Institute for the Developing Brain, Minneapolis, USA (GRID:grid.17635.36) (ISNI:0000 0004 1936 8657); University of Minnesota Medical School, Department of Pediatrics, Minneapolis, USA (GRID:grid.17635.36) (ISNI:0000000419368657); University of Minnesota, Institute of Child Development, College of Education and Human Development, Minneapolis, USA (GRID:grid.17635.36) (ISNI:0000 0004 1936 8657) 
15  University of Pennsylvania, Penn Statistics in Imaging and Visualization Center, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Center for Biomedical Image Computing and Analytics, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972) 
16  Child Mind Institute, Center for the Developing Brain, New York, USA (GRID:grid.428122.f) (ISNI:0000 0004 7592 9033); Nathan Kline Institute for Psychiatric Research, Center for Biomedical Imaging and Neuromodulation, Orangeburg, USA (GRID:grid.250263.0) (ISNI:0000 0001 2189 4777) 
17  University of Pennsylvania, Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Department of Psychiatry, Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Lifespan Brain Institute, Children’s Hospital of Philadelphia and Perelman School of Medicine, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972); University of Pennsylvania, Center for Biomedical Image Computing and Analytics, Philadelphia, USA (GRID:grid.25879.31) (ISNI:0000 0004 1936 8972) 
Pages
3511
Publication year
2024
Publication date
2024
Publisher
Nature Publishing Group
e-ISSN
20411723
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.1038/s41467-024-47748-w
ProQuest document ID
3046096237
Copyright
© The Author(s) 2024. 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.