Early Development of Functional Network Segregation Revealed by Connectomic Analysis of the Preterm Human Brain

Cao, Miao; He, Yong; Dai, Zhengjia; Liao, Xuhong; Jeon, Tina; Ouyang, Minhui; Chalak, Lina F.; Bi, Yanchao; Rollins, Nancy; Dong, Qi; Huang, Hao

doi:10.1093/cercor/bhw038

Cited by 116 publications

(180 citation statements)

References 85 publications

(110 reference statements)

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“…Our results are in line with previous studies where network analysis revealed the rapid increase in network connectivity patterns of the preserved hub and rich-club structures in core connections at the expense of diminished peripheral connections in preterm infants compared to term-born controls [23, 24]. The impact of prematurity on brain network topology preserved core connections between deep gray matter and central cortical regions at term-equivalent age for efficient use of reserved white matter following preterm birth [20].…”

Section: Discussionsupporting

confidence: 93%

Accelerated Small-World Property of Structural Brain Networks in Preterm Infants at Term-Equivalent Age

2018

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Background: The prediction of neurodevelopmental outcomes in preterm infants is one of the clinical challenges of pediatrics. Despite the recent interest in brain development and white matter connectivity using a network-based analysis, very little is known about the brain network of at term-equivalent age in preterm infants. Objective: We aimed to investigate the structural brain network using diffusion MRI following preterm delivery at term-equivalent age compared with term infants and explored the influence of gestational age (GA) and clinical factors. Method: Diffusion tensor imaging data were acquired prospectively from 55 preterm neonates without apparent brain abnormalities (mean gestational age: 29.43 weeks) and 21 full-term infants at term-equivalent age. The global structural brain networks were produced by probabilistic white matter tractography in combination with the Johns Hopkins University neonate atlas to quantify connectivity between different cortical regions. Results: Compared with full-term infants, preterm infants had significantly lower global efficiency (p = 0.048) and increased small worldness (p = 0.012) after correcting for sex and age at MRI scan. The increased small worldness in the brain network at term-equivalent age was significantly linearly correlated with lower GA after adjusting for sex and the effects of postmenstrual age at MRI scan on the data in preterm infants (β = –0.020, p = 0.037). In multivariate analysis, infants with chronic lung disease had significantly decreased changes in clustering (p = 0.014) and local efficiency (p = 0.027). Conclusion: The accelerated small worldness in preterm infants suggests that the structural brain network after preterm birth is reorganized in maximizing integrated and segregated processing, implying resilience against prematurity-associated pathology.

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Section: Discussionsupporting

confidence: 93%

Accelerated Small-World Property of Structural Brain Networks in Preterm Infants at Term-Equivalent Age

2018

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“…Further details are described in Table 4 state functional connectivity study also found that the sensorimotor, auditory, and visual networks were less mature in preterm neonates compared with term newborns (Smyser et al 2010). Indeed, the cortical hubs and their associated cortical networks in neonates are largely located in primary sensory and motor brain regions (Cao et al 2016;Fransson et al 2011;Gao et al 2011), supporting the fact that the perception-action coupling network appears in infants. Our results showed decreased ALFF activity in MLPT newborns in the primary sensory and motor areas, further implying that perception-action behavior is less mature in the MLPT newborns compared with the term newborns.…”

Section: Altered Alff Activity In Mlpt Newbornsmentioning

confidence: 76%

Frequency of Spontaneous BOLD Signal Differences between Moderate and Late Preterm Newborns and Term Newborns

Wei

Wang

et al. 2016

Neurotox Res

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Little is known about the frequency features of spontaneous neural activity in the brains of moderate and late preterm (MLPT) newborns. We used resting-state functional magnetic resonance imaging (rs-fMRI) and the amplitude of low-frequency fluctuation (ALFF) method to investigate the frequency properties of spontaneous blood oxygen level-dependent (BOLD) signals in 26 MLPT and 35 term newborns. Two frequency bands, slow-4 (0.027-0.073 Hz) and slow-5 (0.01-0.027 Hz), were analyzed. Our results showed widespread differences in ALFF between the two bands; differences occurred mainly in the primary sensory and motor cortices and to a lesser extent in association cortices and subcortical areas. Compared with term newborns, MLPT newborns showed significantly altered neural activity predominantly in the primary sensory and motor cortices and in the posterior cingulate gyrus/precuneus. In addition, a significant interaction between frequency bands and groups was observed in the primary somatosensory cortex. Intriguingly, these primary sensory and motor regions have been proven to be the major cortical hubs during the neonatal period. Our results revealed the frequency of spontaneous BOLD signal differences between MLPT and term newborns, which contribute to the understanding of regional development of spontaneous brain rhythms of MLPT newborns.

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“…shown that these networks are present at term-equivalent age 22,23 , and show the greatest 130 maturational changes in healthy term-born infants over the first two years [24][25][26][27][28] . It has, 131 subsequently, been proposed that they might play a crucial role in infant learning and 132 development 29 , even though there is little behavioral manifestation of executive control before 133 5 1/2 months postnatally 30,31 .…”

Section: Neonatal Intensive Care Units (Nicus) 119mentioning

confidence: 97%

Disruption to functional networks in neonates with perinatal brain injury predicts motor skills at 8 months

Linke

Wild

Zubiaurre-Elorza

et al. 2017

Preprint

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ObjectiveFunctional connectivity magnetic resonance imaging (fcMRI) of neonates with perinatal brain injury could improve prediction of motor impairment before symptoms manifest, and establish how early brain organization relates to subsequent development. Methods: This cohort study is the first to describe and quantitatively assess functional brain networks and their relation to later motor skills in neonates with a diverse range of perinatal brain injuries. Infants (n=65, included in final analyses: n=53) were recruited from the neonatal intensive care unit (NICU) and were stratified based on their age at birth (premature vs. term), and on whether neuropathology was diagnosed from structural MRI. Functional brain networks and a measure of disruption to functional connectivity were obtained from 14 minutes of fcMRI acquired during natural sleep at term-equivalent age.ResultsDisruption to connectivity of the somatomotor and frontoparietal executive networks predicted motor impairment at 4 and 8 months. This disruption in functional connectivity was not found to be driven by differences between clinical groups, or by any of the specific measures we captured to describe the clinical course.ConclusionfcMRI was predictive over and above other clinical measures available at discharge from the NICU, including structural MRI. Motor learning was affected by disruption to somatomotor networks, but also frontoparietal executive networks, which supports the functional importance of these networks in early development. Disruption to these two networks might be best addressed by distinct intervention strategies.

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Early Development of Functional Network Segregation Revealed by Connectomic Analysis of the Preterm Human Brain

Cited by 116 publications

References 85 publications

Accelerated Small-World Property of Structural Brain Networks in Preterm Infants at Term-Equivalent Age

Accelerated Small-World Property of Structural Brain Networks in Preterm Infants at Term-Equivalent Age

Frequency of Spontaneous BOLD Signal Differences between Moderate and Late Preterm Newborns and Term Newborns

Disruption to functional networks in neonates with perinatal brain injury predicts motor skills at 8 months

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