A DTI-Based Template-Free Cortical Connectome Study of Brain Maturation

Tymofiyeva, Olga; Hess, Christopher P.; Ziv, Etay; Lee, Patricia N.; Glass, Hannah C.; Ferriero, Donna M.; Barkovich, A. James; Xu, Duan

doi:10.1371/journal.pone.0063310

Cited by 78 publications

(86 citation statements)

References 24 publications

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“…This result is consistent with results from Tymofiyeva et al who found higher small-worldness in infants scanned shortly after normal term birth than in a group of preterm infants scanned at an average of ∼ 35 weeks after conception [52]. In their work, as here, rise in smallworldness was due to increased normalized CC values and stable normalized CPL.…”

Section: Discussionsupporting

confidence: 93%

“…Some other recent works have focused on the examination of the structural connectome of young infants by performing tractography between numerous anatomical regions in the brain [3,41,50,52,53,58,54]. Takahashi et al examined results of full-brain tractography qualitatively and described trends across postmortem infants between 17 and 40 weeks [50].…”

Section: Introductionmentioning

confidence: 99%

“…Yap et al examined the development of connectomes in young children, across a range of ages between 2 weeks and 2 years, using measures of network integration and segregation [58]. Tymofiyeva et al used an atlas-free approach to analyze connectome development in preterm infants, children and adults, also employing network measures to capture topological changes [52,53]. Very recently, Ball et al studied a specific network measure known as rich-club organization in a cohort of preterm infants [2].…”

Section: Introductionmentioning

confidence: 99%

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Structural network analysis of brain development in young preterm neonates

et al. 2014

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Preterm infants develop differently than those born at term and are at higher risk of brain pathology. Thus, an understanding of their development is of particular importance. Diffusion tensor imaging (DTI) of preterm infants offers a window into brain development at a very early age, an age at which that development is not yet fully understood. Recent works have used DTI to analyze structural connectome of the brain scans using network analysis. These studies have shown that, even from infancy, the brain exhibits small-world properties. Here we examine a cohort of 47 normal preterm neonates (i.e., without brain injury and with normal neurodevelopment at 18 months of age) scanned between 27 and 45 weeks post-menstrual age to further the understanding of how the structural connectome develops. We use fullbrain tractography to find white matter tracts between the 90 cortical and sub-cortical regions defined in the University of North Carolina Chapel Hill neonatal atlas. We then analyze the resulting connectomes and explore the differences between weighting edges by tract count versus fractional anisotropy. We observe that the brain networks in preterm infants, much like infants born at term, show high efficiency and clustering measures across a range of network scales. Further, the development of many individual region-pair connections, particularly in the frontal and occipital lobes, is significantly correlated with age. Finally, we observe that the preterm infant connectome remains highly efficient yet becomes more clustered across this age range, leading to a significant increase in its small-world structure.

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Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Structural network analysis of brain development in young preterm neonates

et al. 2014

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“…A number of DWI studies have evaluated postnatal structural brain network development (Hagmann et al, 2012(Hagmann et al, , 2010Huang et al, 2013;Tymofiyeva et al, 2013;Yap et al, 2011) and demonstrated increasing integration and decreasing segregation (or clustering, Box 1) as hallmark features of childhood connectome maturation. Similarly, modules become increasingly interconnected and are further shaped, especially in the earliest postnatal years (Hagmann et al, 2010;Huang et al, 2013).…”

Section: Postnatal Brain Developmentmentioning

confidence: 99%

The emergence of functional architecture during early brain development

2017

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Early human brain development constitutes a sequence of intricate processes resulting in the ontogeny of functionally operative neural circuits. Developmental trajectories of early brain network formation are genetically programmed and can be modified by epigenetic and environmental influences. Such alterations may exert profound effects on neurodevelopment, potentially persisting throughout the lifespan. This review focuses on the critical period of fetal and early postnatal brain development. Here we collate findings from neuroimaging studies, with a particular focus on functional MRI research that interrogated early brain network development in both health and high-risk or disease states. First, we will provide an overview of the developmental processes that take place from the embryonic period through early infancy in order to contextualize brain network formation. Second, functional brain network development in the typically developing brain will be discussed. Third, we will touch on prenatal and perinatal risk factors that may interfere with the trajectories of functional brain wiring, including prenatal substance exposure, maternal mental illness and preterm

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“…Initial studies of neonatal structural networks have reported only dense local connectivity within segregated modules and few long-distance connections (12,15). In contrast, functional MRI reveals large-scale dynamic functional networks analogous to those seen in adults (16,17) and compatible with more advanced cerebral maturation.…”

mentioning

confidence: 97%

Rich-club organization of the newborn human brain

Ball

Aljabar

Zebari

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

333

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Combining diffusion magnetic resonance imaging and network analysis in the adult human brain has identified a set of highly connected cortical hubs that form a "rich club"-a high-cost, highcapacity backbone thought to enable efficient network communication. Rich-club architecture appears to be a persistent feature of the mature mammalian brain, but it is not known when this structure emerges during human development. In this longitudinal study we chart the emergence of structural organization in mid to late gestation. We demonstrate that a rich club of interconnected cortical hubs is already present by 30 wk gestation. Subsequently, until the time of normal birth, the principal development is a proliferation of connections between core hubs and the rest of the brain. We also consider the impact of environmental factors on early network development, and compare term-born neonates to preterm infants at term-equivalent age. Though rich-club organization remains intact following premature birth, we reveal significant disruptions in both in cortical-subcortical connectivity and short-distance corticocortical connections. Rich club organization is present well before the normal time of birth and may provide the fundamental structural architecture for the subsequent emergence of complex neurological functions. Premature exposure to the extrauterine environment is associated with altered network architecture and reduced network capacity, which may in part account for the high prevalence of cognitive problems in preterm infants.connectome | brain development | tractography | preterm birth T o understand the functional properties of a complex network it is necessary to examine its structural organization and topological properties. In the human brain this can be achieved at a macroscale by tracing white matter connections between brain regions with diffusion MRI; this enables the interrogation of structural network topology in vivo with millimeter-scale spatial resolution, providing complementary evidence to experimental studies (1, 2).Network analysis of the adult human structural connectome has revealed a set of highly connected cortical "hubs" predominantly located in heteromodal association cortex, that provide a foundation for coherent neuronal activation across distal cortical regions (3-5). Further, some hub regions tend to be densely connected to each other, forming a "rich club" comprised of frontal and parietal cortex, precuneus, cingulate and the insula, as well as the hippocampus, thalamus, and putamen (6). Rich-club organization has been identified in a number of complex networks (7) and represents an attractive feature for investigation in the brain because rich-club connections tend to dominate network topology (8). Rich-club architecture appears to be a fundamental feature of the mature mammalian brain with similar organization identified in animal models (9, 10).It has been suggested that the emergence of complex neurological function is associated with the integration of major hubs across the cortex (11,...

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A DTI-Based Template-Free Cortical Connectome Study of Brain Maturation

Cited by 78 publications

References 24 publications

Structural network analysis of brain development in young preterm neonates

Structural network analysis of brain development in young preterm neonates

The emergence of functional architecture during early brain development

Rich-club organization of the newborn human brain

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