A generative network model of neurodevelopmental diversity in structural brain organization

• DOI: 10.1038/s41467-021-24430-z
• Publication Date: 2021-07-09T10:03:11Z
• Authors: Danyal Akarca; Petra E. Vértes; Edward T. Bullmore; ; Kate Baker; Susan E. Gathercole; Joni Holmes; Rogier A. Kievit; Tom Manly; Joe Bathelt; Marc Bennett; Giacomo Bignardi; Sarah Bishop; Erica Bottacin; Lara Bridge; Diandra Brkic; Annie Bryant; Sally Butterfield; Elizabeth M. Byrne; Gemma Crickmore; Edwin S. Dalmaijer; Fánchea Daly; Tina Emery; Laura Forde; Grace Franckel; Delia Fuhrmann; Andrew Gadie; Sara Gharooni; Jacalyn Guy; Erin Hawkins; Agnieszka Jarosla...; Sara Joeghan; Amy Johnson; Jonathan Jones; Silvana Mareva; Elise Ng-Cordell; Sinead O’Brien; Cliodhna O’Leary; Joseph P. Rennie; Ivan Simpson-Kent; Roma Siugzdaite; Tess A. Smith; Stephani Uh; Maria Vedechkina; Francesca Woolgar; Natalia Zdorovtsova; Mengya Zhang; Duncan E. Astle
• Keywords: Male; /141; 0301 basic medicine; 570; /631/378/116/1925; Adolescent; Science; Neurogenesis; Models, Neurological; Article; Cohort Studies; 03 medical and health sciences; 0302 clinical medicine; Child Development; Cognition; Humans; Computer Simulation; Child; /631/378/2571/1696; Q; article; Brain; Magnetic Resonance Imaging; /692/617/375/366; /631/553/2712; /9; /59/57; Female; Nerve Net; /119

AbstractThe formation of large-scale brain networks, and their continual refinement, represent crucial developmental processes that can drive individual differences in cognition and which are associated with multiple neurodevelopmental conditions. But how does this organization arise, and what mechanisms drive diversity in organization? We use generative network modeling to provide a computational framework for understanding neurodevelopmental diversity. Within this framework macroscopic brain organization, complete with spatial embedding of its organization, is an emergent property of a generative wiring equation that optimizes its connectivity by renegotiating its biological costs and topological values continuously over time. The rules that govern these iterative wiring properties are controlled by a set of tightly framed parameters, with subtle differences in these parameters steering network growth towards different neurodiverse outcomes. Regional expression of genes associated with the simulations converge on biological processes and cellular components predominantly involved in synaptic signaling, neuronal projection, catabolic intracellular processes and protein transport. Together, this provides a unifying computational framework for conceptualizing the mechanisms and diversity in neurodevelopment, capable of integrating different levels of analysis—from genes to cognition.