Development of human electrophysiological brain networks

Abstract

Functional activity in the human brain is intrinsically organized into independently active, connected brain regions. These networks include sensorimotor systems, as well as higher-order cognitive networks such as the default mode network (DMN), which dominates activity when the brain is at rest, and the frontoparietal (FPN) and salience (SN) networks, which are often engaged during demanding tasks. Evidence from functional magnetic resonance imaging (fMRI) suggests that although sensory systems are mature by the end of childhood, the integrity of the FPN and SN develops throughout adolescence. There has been little work to corroborate these findings with electrophysiology. Using magnetoencephalography (MEG) recordings of 48 participants (aged 9-25 yr) at rest, we find that beta-band functional connectivity within the FPN, SN, and DMN continues to increase through adolescence, whereas connectivity in the visual system is mature by late childhood. In contrast to fMRI results, but replicating the MEG findings of Schäfer et al. (Schäfer CB, Morgan BR, Ye AX, Taylor MJ, Doesburg SM. Hum Brain Mapp 35: 5249-5261, 2014), we also see that connectivity between networks increases rather than decreases with age. This suggests that the development of coordinated beta-band oscillations within and between higher-order cognitive networks through adolescence might contribute to the developing abilities of adolescents to focus their attention and coordinate diverse aspects of mental activity. NEW & NOTEWORTHY Using magnetoencephalography to assess beta frequency oscillations, we show that functional connectivity within higher-order cognitive networks increases from childhood, reaching adult values by age 20 yr. In contrast, connectivity within a primary sensory (visual) network reaches adult values by age 14 yr. In contrast to functional MRI findings, connectivity between cognitive networks matures at a rate similar to within-network connectivity, suggesting that coordination of beta oscillations both within and between networks is associated with maturation of cognitive skills.

Keywords: default mode network; development; frontoparietal network; magnetoencephalography; salience network.

Fig. 1.

The spherical regions of interest (ROIs) that represent the nodes of the 4 networks, displayed using BrainNet Viewer (http://www.nitrc.org/projects/bnv/) (Xia et al. 2013) with the ICBM-152 template brain (Mazziotta et al. 2001b). The ROIs are located symmetrically in the 2 hemispheres. The coordinates of the center of each ROI are specified in Montreal Neurological Institute space according to loci defined in the functional atlas developed by Yeo et al. For each participant, the centers of the ROIs were mapped onto the corresponding location in that individual’s brain as described in materials and methods.

Fig. 2.

Mean connectivity in the beta band in the young adult group (age > 18 yr). Black boxes denote the 3 attentional networks and the visual network. Deep blue denotes zero connectivity; no negative correlations were observed. Connectivity is the Fisher-transformed correlation between amplitude envelopes of 13- to 30-Hz signals, with adjustment to allow for variation between participants in head shape and size. Abbreviations of region names are defined as shown in Fig. 1.

Fig. 3.

A–C: beta-band connectivities averaged across the pairs of regions of interest (ROIs) within each of the 4 networks in adults, adolescents (aged 13–18 yr), and children. D: difference in connectivity between adults and children. Uncorrected P values: *P < 0.05, **P < 0.005, ***P < 0.001. All cells marked ** or *** are significant at the corrected threshold (Bonferroni correction for the 11 comparisons). DMN, default mode network; FPN, frontoparietal network; SN, salience network; VIS, visual network.

Fig. 4.

A: within-network beta-band connectivity for each of our 4 networks as a function of age. Symbols show individual participants, and lines show model fits. DMN, default mode network; FPN, frontoparietal network; SN, salience network; VIS, visual network. Fitted values of the parameter governing the initial rate of increase of connectivity with age (α₃, which has units years⁻¹) are given in the key. B: beta-band connectivity between each pair of cognitive networks as a function of age (DMN-FPN, DMN-SN, FPN-SN) and the mean connectivity between the 3 cognitive networks and the visual network as a function of age (COG-VIS).