Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2011;6(9):e25278.
doi: 10.1371/journal.pone.0025278. Epub 2011 Sep 23.

Temporal and spatial evolution of brain network topology during the first two years of life

Wei Gao  1 , John H Gilmore, Kelly S Giovanello, Jeffery Keith Smith, Dinggang Shen, Hongtu Zhu, Weili Lin
Affiliations

Temporal and spatial evolution of brain network topology during the first two years of life

Wei Gao et al. PLoS One. 2011.

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.

PubMed Disclaimer

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Age-dependent growth pattern of functional connections.
(a) the connection density plot of all three age groups (based on statistical testing of connections (P<0.05, FDR corrected)); (b) the histogram plots of the normalized anatomical distance associated with the significant connections for each age group; (c) statistical comparisons of the anatomical distances associated with those connections that exhibit significantly changed strength with age. Red: increasing connections with age; blue: decreasing connections with age.
Figure 2
Figure 2. The evolution of brain's topology and small-world properties.
(a) The group mean correlation matrices at a cost of 10% are visualized using spring embedding plots for all three groups. Nodes are color coded with respect to the lobe they belong to. Each edge represents the mean connectivity strength between a pair of nodes. The rCL and rCP represent formula imageand formula imagewhere CL and CP are the clustering coefficient and characteristic path length for a given subgraph and the subscript “random” indicates a random network. SW represents the small-worldness measure; (b) Statistical comparison of LE and GE at cost 10% based on individual subject's correlation matrices. Red asterisks represents significant difference at p<0.05 (FDR correction); (c) LE, GE, and CD curve across the cost range of 1% to 50%. Significant increase of LE occurs from neonates to 1 yr olds for a range of cost spanning from 2% through 21% and GE from 4% to 44% (p<0.05, FDR corrected). The calculation was based on individual subjects and the mean values for each age group are plotted.
Figure 3
Figure 3. Regional developments of LE (a), GE (b), nodal maximum connection distance (MD) (c) and Degree (d).
Both regional increase (represented by yellow to red colors) and decrease (represented by green to blue colors) are shown on the same brain surface. The left column shows the changes from neonates to 1 yr olds while the right column shows the changes from 1 yr to 2 yr olds.
Figure 4
Figure 4. The temporal and spatial evolution of brain hubs during the first two years of life.
(a) Spatial distribution of the top 10 hubs and their associated connections at cost 10% (based on the group-mean connectivity matrix) is shown; (b) The degree and maximum connection distance (MD) of the top 10 hubs are compared across different age groups. Red asterisks represents significant difference at p<0.05 (FDR correction).
Figure 5
Figure 5. Brain's resilience to random errors and targeted attacks in comparison with random and scale free networks at cost 10%.
(a) Effects of random errors (left) and targeted attacks (right) on GE; (b) Effects of random errors (left) and targeted attacks (right) on LE. All efficiency values were normalized to the corresponding values of an intact network.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Salvador R, Suckling J, Coleman M, Pickard JD, Menon D, et al. Neurophysiological architecture of functional magnetic resonance images of human brain. Cerebral Cortex. 2005;34:387–413. - PubMed
    1. Achard S, Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput Biol. 2007;3:e17. - PMC - PubMed
    1. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci. 2006;26:63–72. - PMC - PubMed
    1. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186–198. - PubMed
    1. Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, et al. Functional brain networks develop from a ‘local to distributed’ organization. PLoS Comput Biol. 2009;5:e1000381. - PMC - PubMed

Publication types