Temporal and Spatial Evolution of Brain Network Topology during the First Two Years of Life

Wei Gao,John H Gilmore,Dinggang Shen,Hongtu Zhu,Kelly S Giovanello,Jeffery Keith Smith,Weili Lin,Michael Breakspear

doi:10.1371/journal.pone.0025278

Wei Gao, John H Gilmore + Show 6 more

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https://doi.org/10.1371/journal.pone.0025278

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Abstract

The mature brain features high wiring efficiency for information transfer. However, the emerging process of such an efficient topology remains elusive. With resting state functional MRI and a large cohort of normal pediatric subjects (n = 147) imaged during a critical time period of brain development, 3 wk- to 2 yr-old, the temporal and spatial evolution of brain network topology is revealed. The brain possesses the small world topology immediately after birth, followed by a remarkable improvement in whole brain wiring efficiency in 1 yr olds and becomes more stable in 2 yr olds. Regional developments of brain wiring efficiency and the evolution of functional hubs suggest differential development trend for primary and higher order cognitive functions during the first two years of life. Simulations of random errors and targeted attacks reveal an age-dependent improvement of resilience. The lower resilience to targeted attack observed in 3 wk old group is likely due to the fact that there are fewer well-established long-distance functional connections at this age whose elimination might have more profound implications in the overall efficiency of information transfer. Overall, our results offer new insights into the temporal and spatial evolution of brain topology during early brain development.

Highlights

Consisting of billions of neurons and trillions of synapses, the human brain represents perhaps one of the most complex systems in the world
The brain was parcellated into ninety regions-of-interest (ROIs)/nodes encompassing both cortical and subcortical areas [15] (Details in Tables S1 and S2)
Functional connectivity between each pair of ROIs was defined as the magnitude of Pearson correlation of the low frequency (,0.08 Hz) spontaneous blood oxygen level dependent (BOLD) fluctuations

Summary

Introduction

Consisting of billions of neurons and trillions of synapses, the human brain represents perhaps one of the most complex systems in the world. An additional feature of this topology is the presence of highly important brain regions (hubs) that bridge disparate and local clusters to achieve a high global efficiency [8]. Such nodes most likely act as important portals controlling information transfer within the system. Unlike the scale-free network where impairments/attacks targeting hubs lead to profound compromise of brain wiring efficiency, the small world topology possesses high resilience to both random errors and attacks to the hubs [3]

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