Richer than we thought: neurophysiological methods reveal rich-club network development is frequency- and sex-dependent

Marlee M Vandewouw; Elizabeth W Pang; Meng-Chuan Lai; Elizabeth Kelley; Muhammad Ayub; Jason P Lerch; Margot J Taylor; Evdokia Anagnostou

doi:10.1016/j.isci.2023.106384

Richer than we thought: neurophysiological methods reveal rich-club network development is frequency- and sex-dependent

iScience. 2023 Mar 11;26(4):106384. doi: 10.1016/j.isci.2023.106384. eCollection 2023 Apr 21.

Authors

Marlee M Vandewouw^{1

2

3}, Elizabeth W Pang^{4

5}, Meng-Chuan Lai^{4

6

7}, Elizabeth Kelley^{8

9

10}, Muhammad Ayub¹⁰, Jason P Lerch^{4

11

12}, Margot J Taylor^{3

4

13

14}, Evdokia Anagnostou^{1

4

15}

Affiliations

¹ Autism Research Centre, Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, ON M4G 1R8, Canada.
² Institute of Biomedical Engineering, University of Toronto, Toronto, ON M5S 1A1, Canada.
³ Department of Diagnostic Imaging, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.
⁴ Program in Neurosciences and Mental Health, Research Institute, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.
⁵ Division of Neurology, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.
⁶ Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, ON M6J 1H4, Canada.
⁷ Department of Psychiatry, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A1, Canada.
⁸ Department of Psychology, Queen's University, Kingston, ON K7L 3N6 Canada.
⁹ Centre for Neuroscience Studies, Queen's University, Kingston, ON K7L 3N6 Canada.
¹⁰ Department of Psychiatry, Queen's University, Kingston, ON K7L 3N6 Canada.
¹¹ Mouse Imaging Centre, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.
¹² Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, UK.
¹³ Department of Psychology, University of Toronto, Toronto, ON M5S 1A1, Canada.
¹⁴ Department of Medical Imaging, University of Toronto, Toronto, ON M5S 1A1, Canada.
¹⁵ Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A1, Canada.

Abstract

A set of highly connected brain regions called the "rich-club" are vital in integrating information across the functional connectome. Although the literature has identified some changes in rich-club organization with age, little is known about potential sex-specific developmental trajectories, and neurophysiologically relevant frequency-dependent changes have not been established. Here we examine the frequency- and sex-dependent development of rich-club organization using magnetoencephalography in a large normative sample (N = 383) over a wide age span (4-39 years). We report strong divergence between males and females across alpha, beta, and gamma frequencies. While males show increased or no change in rich-club organization with age, females show a consistent, non-linear trajectory that increases through childhood, shifting direction in early adolescence. Using neurophysiological modalities for capturing complex inter-relations between oscillatory dynamics, age, and sex, we establish diverging, sex-specific developmental trajectories of the brain's core functional organization, critically important to our understanding of brain health and disease.

Keywords: Biology of gender; Clinical neuroscience; Developmental biology.