Restricted accessResearch articleFirst published online 2013-02
Growing Trees in Child Brains: Graph Theoretical Analysis of Electroencephalography-Derived Minimum Spanning Tree in 5- and 7-Year-Old Children Reflects Brain Maturation
The child brain is a small-world network, which is hypothesized to change toward more ordered configurations with development. In graph theoretical studies, comparing network topologies under different conditions remains a critical point. Constructing a minimum spanning tree (MST) might present a solution, since it does not require setting a threshold and uses a fixed number of nodes and edges. In this study, the MST method is introduced to examine developmental changes in functional brain network topology in young children. Resting-state electroencephalography was recorded from 227 children twice at 5 and 7 years of age. Synchronization likelihood (SL) weighted matrices were calculated in three different frequency bands from which MSTs were constructed, which represent constructs of the most important routes for information flow in a network. From these trees, several parameters were calculated to characterize developmental change in network organization. The MST diameter and eccentricity significantly increased, while the leaf number and hierarchy significantly decreased in the alpha band with development. Boys showed significant higher leaf number, betweenness, degree and hierarchy and significant lower SL, diameter, and eccentricity than girls in the theta band. The developmental changes indicate a shift toward more decentralized line-like trees, which supports the previously hypothesized increase toward regularity of brain networks with development. Additionally, girls showed more line-like decentralized configurations, which is consistent with the view that girls are ahead of boys in brain development. MST provides an elegant method sensitive to capture subtle developmental changes in network organization without the bias of network comparison.
Get full access to this article
View all access options for this article.
References
1.
Alexander-BlochAF, GogtayN, MeunierD, BirnR, ClasenL, LalondeF, LenrootR, GieddJ, BullmoreET. 2010. Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Front Syst Neurosci, 4:147.
2.
BarryRJ, ClarkeAR, McCarthyR, SelikowitzM, JohnstoneSJ, RushbyJA. 2004. Age and gender effects in EEG coherence: I. Developmental trends in normal children. Clin Neurophysiol, 115:2252–2258.
3.
Bie deHM, BoersmaM, AdriaanseS, VeltmanDJ, WinkAM, RoosendaalSD, BarkhofF, StamCJ, OostromKJ, Delemarre-van de WaalHA, Sanz-ArigitaEJ. 2012. Resting-state networks in awake five- to eight-year old children. Hum Brain Mapp, 33:1189–1201.
4.
BoersmaM, SmitDJ, de BieHM, van BaalGC, BoomsmaDI, de GeusEJ, Delemarre-van de WaalHA, StamCJ. 2011. Network analysis of resting state EEG in the developing young brain: structure comes with maturation. Hum Brain Mapp, 32:413–425.
5.
BoomsmaDI, de GeusEJ, VinkJM, StubbeJH, DistelMA, HottengaJJ, PosthumaD, Van BeijsterveldtTC, HudziakJJ, BartelsM, WillemsenG. 2006. Netherlands Twin Register: From twins to twin families. Twin Res Hum Genet, 9:849–857.
6.
BoomsmaDI, OrlebekeJF, van BaalGC. 1992. The Dutch Twin Register: Growth data on weight and height. Behav Genet, 22:247–251.
7.
BoomsmaDI, van BaalGC. 1998. Genetic influences on childhood IQ in 5- and 7-year-old Dutch twins. Developmental Neuropsychology, 14:115–126.
8.
BullmoreE, SpornsO. 2012. The economy of brain network organization. Nat Rev Neurosci, 13:336–349.
9.
ChenAC, FengW, ZhaoH, YinY, WangP. 2008. EEG default mode network in the human brain: spectral regional field powers. Neuroimage, 41:561–574.
10.
CiftciK. 2011. Minimum spanning tree reflects the alterations of the default mode network during Alzheimer's disease. Ann Biomed Eng, 39:1493–1504.
11.
CourchesneE, PierceK. 2005. Brain overgrowth in autism during a critical time in development: implications for frontal pyramidal neuron and interneuron development and connecitivty. Int J Dev Neurosci, 23:153–170.
12.
FairDA, CohenAL, PowerJD, DosenbachNUF, ChurchJA, MiezinFM, SchlaggarBL, PetersenSE. 2009. Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol, 5:e1000381.
13.
FairDA, DosenbachNU, ChurchJA, CohenAL, BrahmbhattS, MiezinFM, BarchDM, RaichleME, PetersenSE, SchlaggarBL. 2007. Development of distinct control networks through segregation and integration. Proc Natl Acad Sci U S A, 104:13507–13512.
14.
FlavellSW, GreenbergME. 2008. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci, 31:563–590.
15.
GongG, HeY, ConchaL, LebelC, GrossDW, EvansAC, BeaulieuC. 2009. Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cereb Cortex, 19:524–536.
16.
GootjesL, BoumaA, Van StrienJW, ScheltensP, StamCJ. 2006. Attention modulates hemispheric differences in functional connectivity: evidence from MEG recordings. Neuroimage, 30:245–253.
17.
HagmannP, SpornsO, MadanN, CammounL, PienaarR, WedeenVJ, MeuliR, ThiranJP, GrantPE. 2010. White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci U S A, 107:19067–19072.
18.
HuttenlocherPR. 1984. Synapse elimination and plasticity in developing human cerebral cortex. Am J Ment Defic, 88:488–496.
19.
HwangK, HallquistMN, KunaB. 2012. The development of hub architecture in the human functional brain network. Cereb Cortex[Epub ahead of print].10.1093/cercor/bhs227
20.
JasperHH. 1958. Report of the committee on methods of clinical examination in electroencephalography. Electroencephalogr Clin Neurophysiol, 10:370–375.
21.
JoudakiA, SalehiN, JaliliM, KnyazevaMG. 2012. EEG-based functional brain networks: does the network size matter?PLoS One, 7:e35673.
22.
JustMA, KellerTA, MalaveVL, KanaRK, VarmaS. 2012. Autism as a neural systems disorder: a theory of frontal-posterior underconnectivity. Neurosci Biobehav Rev, 36:1292–1313.
23.
KnyazevGG, Slobodskoj-PlusninJY, BocharovAV, PylkovaLV. 2011. The default mode network and EEG alpha oscillations: an independent component analysis. Brain Res, 1402:67–79.
24.
KruskalJB. On the Shortest Spanning Subtree of a Graph and the Traveling Salesman Problem. 1956. Proceedings of the American Mathematical Society, 7:48–50.
25.
LebelC, WalkerL, LeemansA, PhillipsL, BeaulieuC. 2008. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage, 40:1044–1055.
26.
LeeU, KimS, JungKY. 2006. Classification of epilepsy types through global network analysis of scalp electroencephalograms. Phys Rev E Stat Nonlin Soft Matter Phys, 73:041920.
27.
LeeU, OhG, KimS, NohG, ChoiB, MashourGA. 2010. Brain networks maintain a scale-free organization across consciousness, anesthesia, and recovery: evidence for adaptive reconfiguration. Anesthesiology, 113:1081–1091.
OrtegaGJ, SolaRG, PastorJ. 2008. Complex network analysis of human ECoG data. Neurosci Lett, 447:129–133.
35.
PeperJS, KoolschijnPC. 2012. Sex steroids and the organization of the human brain. J Neurosci, 32:6745–6746.
36.
PeperJS, van den HeuvelMP, MandlRC, PolHE, van HonkJ. 2011. Sex steroids and connectivity in the human brain: a review of neuroimaging studies. Psychoneuroendocrinology, 36:1101–1113.
37.
PivikRT, BroughtonRJ, CoppolaR, DavidsonRJ, FoxN, NuwerMR. 1993. Guidelines for the recording and quantitative analysis of electroencephalographic activity in research contexts. Psychophysiology, 30:547–558.
38.
PowerJD, FairDA, SchlaggarBL, PetersenSE. 2010. The development of human functional brain networks. Neuron, 67:735–748.
39.
SadaghianiS, ScheeringaR, LehongreK, MorillonB, GiraudAL, D'EspositoM, KleinschmidtA. 2012. Alpha-band phase synchrony is related to activity in the fronto-parietal adaptive control network. J Neurosci, 32:14305–14310.
40.
SchoenW, ChangJS, LeeU, BobP, MashourGA. 2011. The temporal organization of functional brain connectivity is abnormal in schizophrenia but does not correlate with symptomatology. Conscious Cogn, 20:1050–1054.
41.
SchoonheimMM, HulstHE, LandiD, CiccarelliO, RoosendaalSD, Sanz-ArigitaEJ, VrenkenH, PolmanCH, StamCJ, BarkhofF, GeurtsJJ. 2011. Gender-related differences in functional connectivity in multiple sclerosis. Mult Scler, 18:164–173.
42.
SmitDJ, BoersmaM, SchnackHG, MicheloyannisS, BoomsmaDI, Hulshoff PolHE, StamCJ, de GeusEJ. 2012. The brain matures with stronger functional connectivity and decreased randomness of its network. PLoS ONE, 7:e36896.
43.
SmitDJ, BoersmaM, van BeijsterveldtCE, PosthumaD, BoomsmaDI, StamCJ, de GeusEJ. 2010. Endophenotypes in a dynamically connected brain. Behav Genet, 40:167–177.
44.
SmitDJA, StamCJ, PosthumaD, BoomsmaDI, de GeusEJC. 2008. Heritability of “small-world” networks in the brain: a graph theoretical analysis of resting-state EEG functional connectivity. Hum Brain Mapp, 29:1368–1378.
45.
StamCJ, de HaanW, DaffertshoferA, JonesBF, ManshandenI, van Cappellen van WalsumAM, MontezT, VerbuntJPA, de MunckJC, van DijkBW, BerendseHW, ScheltensP. 2009. Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. Brain, 132:213–224.
46.
StamCJ, NolteG, DaffertshoferA. 2007. Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources. Hum Brain Mapp, 28:1178–1193.
47.
StamCJ, van DijkBW. 2002. Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets. Physica D-Nonlinear Phenomena, 163:236–251.
48.
StamCJ, van StraatenEC. 2012a. Go with the flow: use of a directed phase lag index (dPLI) to characterize patterns of phase relations in a large-scale model of brain dynamics. Neuroimage, 62:1415–1428.
49.
StamCJ, van StraatenEC. 2012b. The organization of physiological brain networks. Clin Neurophysiol, 123:1067–1087.
50.
SupekarK, MusenM, MenonV. 2009. Development of large-scale functional brain networks in children. PLoS Biol, 7:e1000157.
51.
SupekarK, UddinLQ, PraterK, AminH, GreiciusMD, MenonV. 2010. Development of functional and structural connectivity within the default mode network in young children. Neuroimage, 52:290–301.
52.
TamnesCK, OstbyY, FjellAM, WestlyeLT, Due-TonnessenP, WalhovdKB. 2010. Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex, 20:534–548.
53.
ThatcherRW. 1992. Cyclic cortical reorganization during early childhood. Brain Cogn, 20:24–50.
54.
ThatcherRW, NorthDM, BiverCJ. 2008. Development of cortical connections as measured by EEG coherence and phase delays. Hum Brain Mapp, 29:1400–1415.
55.
ThatcherRW, NorthDM, BiverCJ. 2009. Self-organized criticality and the development of EEG phase reset. Hum Brain Mapp, 30:553–574.
TomasiD, VolkowND. 2012. Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psych, 71:443–450.
58.
UddinLQ, SupekarK, MenonV. 2010. Typical and atypical development of functional human brain networks: insights from resting-state FMRI. Front Syst Neurosci, 21:4–21.
59.
UddinLQ, SupekarKS, RyaliS, MenonV. 2011. Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development. J Neurosci, 31:18578–18589.
60.
van BaalGC, BoomsmaDI, de GeusEJ. 2001. Longitudinal genetic analysis of EEG coherence in young twins. Behav Genet, 31:637–651.
61.
van BaalGC, de GeusEJ, BoomsmaDI. 1996. Genetic architecture of EEG power spectra in early life. Electroencephalogr Clin Neurophysiol, 98:502–514.
62.
van den HeuvelMP, StamCJ, KahnRS, Hulshoff PolHE. 2009. Efficiency of functional brain networks and intellectual performance. J Neurosci, 29:7619–7624.
63.
van SteenM. 2010. Graph Theory and Complex Networks: An Introduction. Maarten van Steen.
64.
van WijkBC, StamCJ, DaffertshoferA. 2010. Comparing brain networks of different size and connectivity density using graph theory. PLoS ONE, 5:e13701.
65.
VolpeJJ. 2000. Overview: normal and abnormal human brain development. Ment Retard Dev Disabil Res Rev, 6:1–5.
66.
WangH, HernandezJM, VanMP. 2008. Betweenness centrality in a weighted network. Phys Rev E Stat Nonlin Soft Matter Phys, 77:046105.
67.
YapPT, FanY, ChenY, GilmoreJH, LinW, ShenD. 2011. Development trends of white matter connectivity in the first years of life. PLoS ONE, 6:e24678.
68.
ZhuC, GuoX, JinZ, SunJ, QiuY, ZhuY, TongS. 2011. Influences of brain development and ageing on cortical interactive networks. Clin Neurophysiol, 122:278–283.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
