Developmental Connectomics from Infancy through Early Childhood

Miao Cao, Hao Huang, Yong He, Miao Cao, Hao Huang, Yong He

Abstract

The human brain undergoes rapid growth in both structure and function from infancy through early childhood, and this significantly influences cognitive and behavioral development in later life. A newly emerging research framework, developmental connectomics, provides unprecedented opportunities for exploring the developing brain through non-invasive mapping of structural and functional connectivity patterns. Within this framework, we review recent neuroimaging and neurophysiological studies investigating connectome development from 20 postmenstrual weeks to 5 years of age. Specifically, we highlight five fundamental principles of brain network development during the critical first years of life, emphasizing strengthened segregation/integration balance, a remarkable hierarchical order from primary to higher-order regions, unparalleled structural and functional maturations, substantial individual variability, and high vulnerability to risk factors and developmental disorders.

Keywords: connectome; developmental disorder; functional connectivity; graph theory; segregation and integration; structural connectivity.

Copyright © 2017 Elsevier Ltd. All rights reserved.

Figures

Figure 1. Research summary of developmental connectomics…
Figure 1. Research summary of developmental connectomics from infancy to early childhood
Summary of the developmental brain connectomic studies from early infancy to childhood with advanced neuroimaging and neurophysiological techniques. This figure represents the literature search results on Pubmed (www.ncbi.nlm.nih.gov/pubmed) with keywords “connectivity” OR “network” OR “connectome” combined with “early development” OR “infant” OR “baby”. A total of 112 relevant studies published between 2007 and 2017 are included here. The publications are summarized and plotted as distribution histograms according to their publication years (a), age span (b), imaging modality (c) as well as pie charts regarding sample size (d), sample design (e), and scanning status (f). sMRI, structural MRI; dMRI, diffussion MRI; fMRI, functional MRI; EEG, electroencephalography; fNIRS, functional near-infrared spectroscopy.
Figure 2. Hypothetic models of the brain…
Figure 2. Hypothetic models of the brain connectome development from infancy to early childhood
(a) Presenting the hypothetic developmental model of information segregation and integration in the brain networks. (b) Presenting the hypothetic developmental model from primary regions to high-order association regions. (c) Presenting the hypothetic developmental model of structural and functional brain connectomes.
Figure I
Figure I

References

    1. Tiedemann E. Anatomie und Bildungsgeschichte des Gehirns im Foetus des menschen. Steinische Buchhandlung 1816
    1. Cao M, et al. Toward Developmental Connectomics of the Human Brain. Front Neuroanat. 2016;10:25.
    1. Sporns O, Tononi G, Kötter R. The Human Connectome: A Structural Description of the Human Brain. PLoS Computational Biology. 2005;1:e42.
    1. Kelly C, et al. Characterizing variation in the functional connectome: promise and pitfalls. Trends Cogn Sci. 2012;16:181–8.
    1. Watts DJ, Strogatz SH. Collective dynamics of ‘small-world’ networks. Nature. 1998;393:440–2.
    1. Bullmore E, Sporns O. The economy of brain network organization. Nat Rev Neurosci. 2012;13:336–49.
    1. Fransson P, et al. The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb Cortex. 2011;21:145–54.
    1. van den Heuvel MP, et al. The Neonatal Connectome During Preterm Brain Development. Cereb Cortex. 2015;25:3000–13.
    1. Cao M, et al. Early Development of Functional Network Segregation Revealed by Connectomic Analysis of the Preterm Human Brain. Cereb Cortex 2016
    1. Gao W, et al. Temporal and spatial evolution of brain network topology during the first two years of life. PLoS One. 2011;6:e25278.
    1. Nie J, et al. Longitudinal development of cortical thickness, folding, and fiber density networks in the first 2 years of life. Hum Brain Mapp. 2014;35:3726–37.
    1. Hagmann P, et al. White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci U S A. 2010;107:19067–72.
    1. Fan Y, et al. Brain anatomical networks in early human brain development. Neuroimage. 2011;54:1862–71.
    1. Huang H, et al. Development of human brain structural networks through infancy and childhood. Cereb Cortex. 2015;25:1389–404.
    1. Brown CJ, et al. Structural network analysis of brain development in young preterm neonates. Neuroimage. 2014;101:667–80.
    1. Tymofiyeva O, et al. A DTI-based template-free cortical connectome study of brain maturation. PLoS One. 2013;8:e63310.
    1. van den Heuvel MP, Sporns O. Network hubs in the human brain. Trends Cogn Sci. 2013;17:683–96.
    1. Ball G, et al. Rich-club organization of the newborn human brain. Proc Natl Acad Sci U S A. 2014;111:7456–61.
    1. Colizza V, et al. Detecting rich-club ordering in complex networks. Nature Physics. 2006;2:110–115.
    1. van den Heuvel MP, Sporns O. Rich-club organization of the human connectome. J Neurosci. 2011;31:15775–86.
    1. Thomason ME, et al. Intrinsic functional brain architecture derived from graph theoretical analysis in the human fetus. PLoS One. 2014;9:e94423.
    1. Yap PT, et al. Development trends of white matter connectivity in the first years of life. PLoS One. 2011;6:e24678.
    1. Fair DA, et al. Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol. 2009;5:e1000381.
    1. Damaraju E, et al. Functional connectivity in the developing brain: a longitudinal study from 4 to 9months of age. Neuroimage. 2014;84:169–80.
    1. Thomason ME, et al. Age-related increases in long-range connectivity in fetal functional neural connectivity networks in utero. Dev Cogn Neurosci. 2015;11:96–104.
    1. Omidvarnia A, et al. Functional bimodality in the brain networks of preterm and term human newborns. Cereb Cortex. 2014;24:2657–68.
    1. Qiu A, Mori S, Miller MI. Diffusion tensor imaging for understanding brain development in early life. Annu Rev Psychol. 2015;66:853–76.
    1. Huang H, Vasung L. Gaining insight of fetal brain development with diffusion MRI and histology. Int J Dev Neurosci. 2014;32:11–22.
    1. Huang H, et al. Anatomical characterization of human fetal brain development with diffusion tensor magnetic resonance imaging. J Neurosci. 2009;29:4263–73.
    1. Takahashi E, et al. Emerging cerebral connectivity in the human fetal brain: an MR tractography study. Cereb Cortex. 2012;22:455–64.
    1. Huang H, et al. White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage. 2006;33:27–38.
    1. Dubois J, et al. Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum Brain Mapp. 2008;29:14–27.
    1. Gao W, et al. Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am J Neuroradiol. 2009;30:290–6.
    1. Huang H, et al. Coupling diffusion imaging with histological and gene expression analysis to examine the dynamics of cortical areas across the fetal period of human brain development. Cereb Cortex. 2013;23:2620–31.
    1. Yu Q, et al. Structural Development of Human Fetal and Preterm Brain Cortical Plate Based on Population-Averaged Templates. Cereb Cortex 2015
    1. Ball G, et al. Development of cortical microstructure in the preterm human brain. Proc Natl Acad Sci U S A. 2013;110:9541–6.
    1. Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol. 1997;387:167–78.
    1. Gilmore JH, et al. Longitudinal development of cortical and subcortical gray matter from birth to 2 years. Cereb Cortex. 2012;22:2478–85.
    1. Li G, et al. Measuring the dynamic longitudinal cortex development in infants by reconstruction of temporally consistent cortical surfaces. Neuroimage. 2014;90:266–79.
    1. Lyall AE, et al. Dynamic Development of Regional Cortical Thickness and Surface Area in Early Childhood. Cereb Cortex. 2015;25:2204–12.
    1. Li G, et al. Mapping region-specific longitudinal cortical surface expansion from birth to 2 years of age. Cereb Cortex. 2013;23:2724–33.
    1. Nie J, et al. A computational growth model for measuring dynamic cortical development in the first year of life. Cereb Cortex. 2012;22:2272–84.
    1. Li G, et al. Mapping longitudinal development of local cortical gyrification in infants from birth to 2 years of age. J Neurosci. 2014;34:4228–38.
    1. Geng X, et al. Structural and Maturational Covariance in Early Childhood Brain Development. Cereb Cortex 2016
    1. Rilling JK, et al. The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci. 2008;11:426–8.
    1. Hill J, et al. Similar patterns of cortical expansion during human development and evolution. Proc Natl Acad Sci U S A. 2010;107:13135–40.
    1. Fransson P, et al. Resting-state networks in the infant brain. Proc Natl Acad Sci U S A. 2007;104:15531–6.
    1. Doria V, et al. Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci U S A. 2010;107:20015–20.
    1. Gao W, et al. Evidence on the emergence of the brain’s default network from 2-week-old to 2-year-old healthy pediatric subjects. Proc Natl Acad Sci U S A. 2009;106:6790–5.
    1. Jakab A, et al. Fetal functional imaging portrays heterogeneous development of emerging human brain networks. Front Hum Neurosci. 2014;8:852.
    1. Gao W, et al. Functional Network Development During the First Year: Relative Sequence and Socioeconomic Correlations. Cereb Cortex. 2015;25:2919–28.
    1. Gao W, et al. Development of human brain cortical network architecture during infancy. Brain Struct Funct. 2015;220:1173–86.
    1. Alcauter S, et al. Development of thalamocortical connectivity during infancy and its cognitive correlations. J Neurosci. 2014;34:9067–75.
    1. Toulmin H, et al. Specialization and integration of functional thalamocortical connectivity in the human infant. Proc Natl Acad Sci U S A. 2015;112:6485–90.
    1. Chugani HT. A critical period of brain development: studies of cerebral glucose utilization with PET. Prev Med. 1998;27:184–8.
    1. Liang X, et al. Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain. Proc Natl Acad Sci U S A. 2013;110:1929–34.
    1. Tomasi D, Wang GJ, Volkow ND. Energetic cost of brain functional connectivity. Proc Natl Acad Sci U S A. 2013;110:13642–7.
    1. Wang Z, et al. Understanding structural-functional relationships in the human brain: a large-scale network perspective. Neuroscientist. 2015;21:290–305.
    1. Park HJ, Friston K. Structural and functional brain networks: from connections to cognition. Science. 2013;342:1238411.
    1. Liao X, et al. Spontaneous functional network dynamics and associated structural substrates in the human brain. Front Hum Neurosci. 2015;9:478.
    1. Song S, Miller KD, Abbott LF. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci. 2000;3:919–26.
    1. Mueller S, et al. Individual variability in functional connectivity architecture of the human brain. Neuron. 2013;77:586–95.
    1. Finn ES, et al. Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat Neurosci. 2015;18:1664–71.
    1. Zhong S, He Y, Gong G. Convergence and divergence across construction methods for human brain white matter networks: an assessment based on individual differences. Hum Brain Mapp. 2015;36:1995–2013.
    1. Gao W, et al. Intersubject variability of and genetic effects on the brain’s functional connectivity during infancy. J Neurosci. 2014;34:11288–96.
    1. Lee SJ, et al. Quantitative tract-based white matter heritability in twin neonates. Neuroimage. 2015;111:123–35.
    1. Graham AM, et al. Implications of newborn amygdala connectivity for fear and cognitive development at 6-months-of-age. Dev Cogn Neurosci. 2016;18:12–25.
    1. Alcauter S, et al. Frequency of spontaneous BOLD signal shifts during infancy and correlates with cognitive performance. Dev Cogn Neurosci. 2015;12:40–50.
    1. Kuhn-Popp N, et al. Left hemisphere EEG coherence in infancy predicts infant declarative pointing and preschool epistemic language. Soc Neurosci. 2016;11:49–59.
    1. Ball G, et al. Thalamocortical Connectivity Predicts Cognition in Children Born Preterm. Cereb Cortex. 2015;25:4310–8.
    1. Wee CY, et al. Neonatal neural networks predict children behavioral profiles later in life. Hum Brain Mapp 2016
    1. Ball G, et al. The influence of preterm birth on the developing thalamocortical connectome. Cortex. 2013;49:1711–21.
    1. Kwon SH, et al. Adaptive mechanisms of developing brain: cerebral lateralization in the prematurely-born. Neuroimage. 2015;108:144–50.
    1. Thompson DK, et al. Structural connectivity relates to perinatal factors and functional impairment at 7years in children born very preterm. Neuroimage. 2016;134:328–37.
    1. Scheinost D, et al. Preterm birth alters neonatal, functional rich club organization. Brain Struct Funct. 2016;221:3211–22.
    1. Smyser CD, et al. Resting-State Network Complexity and Magnitude Are Reduced in Prematurely Born Infants. Cereb Cortex. 2016;26:322–33.
    1. Batalle D, et al. Early development of structural networks and the impact of prematurity on brain connectivity. Neuroimage. 2017;149:379–392.
    1. Kim DJ, et al. Longer gestation is associated with more efficient brain networks in preadolescent children. Neuroimage. 2014;100:619–27.
    1. Salzwedel AP, et al. Prenatal drug exposure affects neonatal brain functional connectivity. J Neurosci. 2015;35:5860–9.
    1. Li Z, et al. Prenatal cocaine exposure alters functional activation in the ventral prefrontal cortex and its structural connectivity with the amygdala. Psychiatry Res. 2013;213:47–55.
    1. Grewen K, Salzwedel AP, Gao W. Functional Connectivity Disruption in Neonates with Prenatal Marijuana Exposure. Front Hum Neurosci. 2015;9:601.
    1. Kim DJ, et al. Prenatal Maternal Cortisol Has Sex-Specific Associations with Child Brain Network Properties. Cereb Cortex 2016
    1. Graham AM, et al. Early life stress is associated with default system integrity and emotionality during infancy. J Child Psychol Psychiatry. 2015;56:1212–22.
    1. Qiu A, et al. Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants. Transl Psychiatry. 2015;5:e508.
    1. Soe NN, et al. Pre- and Post-Natal Maternal Depressive Symptoms in Relation with Infant Frontal Function, Connectivity, and Behaviors. PLoS One. 2016;11:e0152991.
    1. Di Martino A, et al. Unraveling the Miswired Connectome: A Developmental Perspective. Neuron. 2014;83:1335–1353.
    1. Keehn B, et al. Functional connectivity in the first year of life in infants at-risk for autism: a preliminary near-infrared spectroscopy study. Front Hum Neurosci. 2013;7:444.
    1. Ouyang M, et al. Atypical age-dependent effects of autism on white matter microstructure in children of 2-7 years. Hum Brain Mapp. 2016;37:819–32.
    1. Lewis JD, et al. Network inefficiencies in autism spectrum disorder at 24 months. Transl Psychiatry. 2014;4:e388.
    1. Hughes EJ, et al. A dedicated neonatal brain imaging system. Magn Reson Med 2016
    1. Ball G, et al. An optimised tract-based spatial statistics protocol for neonates: applications to prematurity and chronic lung disease. Neuroimage. 2010;53:94–102.
    1. van den Heuvel MI, Thomason ME. Functional Connectivity of the Human Brain in Utero. Trends Cogn Sci. 2016;20:931–939.
    1. Power JD, et al. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage. 2012;59:2142–54.
    1. Gao W, et al. Functional Connectivity of the Infant Human Brain: Plastic and Modifiable. Neuroscientist 2016
    1. Oishi K, et al. Multi-contrast human neonatal brain atlas: application to normal neonate development analysis. Neuroimage. 2011;56:8–20.
    1. Fonov V, et al. Unbiased average age-appropriate atlases for pediatric studies. Neuroimage. 2011;54:313–27.
    1. Wright R, et al. Construction of a fetal spatio-temporal cortical surface atlas from in utero MRI: Application of spectral surface matching. Neuroimage. 2015;120:467–80.
    1. Glasser MF, et al. A multi-modal parcellation of human cerebral cortex. Nature. 2016;536:171–8.
    1. Mishra V, et al. Differences of inter-tract correlations between neonates and children around puberty: a study based on microstructural measurements with DTI. Front Hum Neurosci. 2013;7:721.
    1. Xia M, He Y. Functional connectomics from a “big data” perspective. NeuroImage 2017

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner