Functional connectivity development along the sensorimotor-association axis enhances the cortical hierarchy

Audrey C Luo; Valerie J Sydnor; Adam Pines; Bart Larsen; Aaron F Alexander-Bloch; Matthew Cieslak; Sydney Covitz; Andrew A Chen; Nathalia Bianchini Esper; Eric Feczko; Alexandre R Franco; Raquel E Gur; Ruben C Gur; Audrey Houghton; Fengling Hu; Arielle S Keller; Gregory Kiar; Kahini Mehta; Giovanni A Salum; Tinashe Tapera; Ting Xu; Chenying Zhao; Taylor Salo; Damien A Fair; Russell T Shinohara; Michael P Milham; Theodore D Satterthwaite

doi:10.1038/s41467-024-47748-w

Functional connectivity development along the sensorimotor-association axis enhances the cortical hierarchy

Nat Commun. 2024 Apr 25;15(1):3511. doi: 10.1038/s41467-024-47748-w.

Authors

Audrey C Luo^{1

2

3}, Valerie J Sydnor^{1

2

3}, Adam Pines^{1

2

3

4}, Bart Larsen^{1

2

3

5

6}, Aaron F Alexander-Bloch^{2

3

7}, Matthew Cieslak^{1

2

3}, Sydney Covitz^{1

2

3}, Andrew A Chen⁸, Nathalia Bianchini Esper⁹, Eric Feczko⁹, Alexandre R Franco^{9

10

11}, Raquel E Gur^{2

3

7}, Ruben C Gur^{2

3}, Audrey Houghton⁵, Fengling Hu^{12

13}, Arielle S Keller^{1

2

3}, Gregory Kiar⁹, Kahini Mehta^{1

2

3}, Giovanni A Salum^{9

14}, Tinashe Tapera^{1

2

3

15}, Ting Xu⁹, Chenying Zhao^{1

2

3

16}, Taylor Salo^{1

2

3}, Damien A Fair^{5

6

17}, Russell T Shinohara^{12

13

18}, Michael P Milham^{9

10}, Theodore D Satterthwaite^{19

20

21

22}

Affiliations

¹ Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
² Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
³ Lifespan Brain Institute, Children's Hospital of Philadelphia and Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
⁴ Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, 94305, USA.
⁵ Masonic Institute for the Developing Brain, University of Minnesota, Minneapolis, MN, 55455, USA.
⁶ Department of Pediatrics, University of Minnesota Medical School, Minneapolis, MN, 55455, USA.
⁷ Department of Child and Adolescent Psychiatry and Behavioral Science, Children's Hospital of Philadelphia, Philadelphia, PA, 19104, USA.
⁸ Division of Biostatistics and Bioinformatics, Department of Public Health Sciences, Medical University of South Carolina, Charleston, SC, 29425, USA.
⁹ Center for the Developing Brain, Child Mind Institute, New York, NY, 10022, USA.
¹⁰ Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, 10962, USA.
¹¹ Department of Psychiatry, NYU Grossman School of Medicine, New York, NY, 10016, USA.
¹² Penn Statistics in Imaging and Visualization Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
¹³ Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
¹⁴ Section on Negative Affect and Social Processes, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
¹⁵ Khoury College of Computer Sciences, Northeastern University, Boston, MA, 02115, USA.
¹⁶ Department of Bioengineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA, 19104, USA.
¹⁷ Institute of Child Development, College of Education and Human Development, University of Minnesota, Minneapolis, MN, 55455, USA.
¹⁸ Center for Biomedical Image Computing and Analytics, University of Pennsylvania, Philadelphia, PA, 19104, USA.
¹⁹ Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA. sattertt@pennmedicine.upenn.edu.
²⁰ Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA. sattertt@pennmedicine.upenn.edu.
²¹ Lifespan Brain Institute, Children's Hospital of Philadelphia and Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA. sattertt@pennmedicine.upenn.edu.
²² Center for Biomedical Image Computing and Analytics, University of Pennsylvania, Philadelphia, PA, 19104, USA. sattertt@pennmedicine.upenn.edu.

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.

Publication types

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

MeSH terms

Adolescent
Adult
Cerebral Cortex / diagnostic imaging
Cerebral Cortex / growth & development
Cerebral Cortex / physiology
Child
Child, Preschool
Connectome*
Female
Humans
Magnetic Resonance Imaging*
Male
Nerve Net / diagnostic imaging
Nerve Net / physiology
Neural Pathways / physiology
Sensorimotor Cortex* / diagnostic imaging
Sensorimotor Cortex* / physiology
Young Adult

Abstract

Publication types

MeSH terms

Grants and funding