Developmental Trajectories and Differences in Functional Brain Network Properties of Preterm and At‐Term Neonates
ABSTRACT Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting‐state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence...
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| Published in | Human brain mapping Vol. 46; no. 1; pp. e70126 - n/a |
|---|---|
| Main Authors | , |
| Format | Journal Article |
| Language | English |
| Published |
Hoboken, USA
John Wiley & Sons, Inc
01.01.2025
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| Online Access | Get full text |
| ISSN | 1065-9471 1097-0193 1097-0193 |
| DOI | 10.1002/hbm.70126 |
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| Abstract | ABSTRACT
Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting‐state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at‐term (n = 332) and preterm (n = 115) neonates at term‐equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow‐up for some preterm participants, we characterized the developmental trajectories for preterm and at‐term neonates, for this purpose linear, quadratic, and log‐linear mixed models were constructed with gestational age at scan as an independent fixed‐effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term‐equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non‐linear developmental trajectories for premature neonates, but decreased integration and segregation even at term‐equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth.
Our results show nonlinear developmental trajectories for different measures of graph theory in preterm infants, but decreased integration and segregation even at term‐equivalent age. |
|---|---|
| AbstractList | Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting‐state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at‐term (n = 332) and preterm (n = 115) neonates at term‐equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow‐up for some preterm participants, we characterized the developmental trajectories for preterm and at‐term neonates, for this purpose linear, quadratic, and log‐linear mixed models were constructed with gestational age at scan as an independent fixed‐effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term‐equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non‐linear developmental trajectories for premature neonates, but decreased integration and segregation even at term‐equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth. Our results show nonlinear developmental trajectories for different measures of graph theory in preterm infants, but decreased integration and segregation even at term‐equivalent age. Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting‐state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at‐term ( n = 332) and preterm ( n = 115) neonates at term‐equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow‐up for some preterm participants, we characterized the developmental trajectories for preterm and at‐term neonates, for this purpose linear, quadratic, and log‐linear mixed models were constructed with gestational age at scan as an independent fixed‐effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term‐equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non‐linear developmental trajectories for premature neonates, but decreased integration and segregation even at term‐equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth. ABSTRACT Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting‐state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at‐term (n = 332) and preterm (n = 115) neonates at term‐equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow‐up for some preterm participants, we characterized the developmental trajectories for preterm and at‐term neonates, for this purpose linear, quadratic, and log‐linear mixed models were constructed with gestational age at scan as an independent fixed‐effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term‐equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non‐linear developmental trajectories for premature neonates, but decreased integration and segregation even at term‐equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth. Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting-state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at-term (n = 332) and preterm (n = 115) neonates at term-equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow-up for some preterm participants, we characterized the developmental trajectories for preterm and at-term neonates, for this purpose linear, quadratic, and log-linear mixed models were constructed with gestational age at scan as an independent fixed-effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term-equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non-linear developmental trajectories for premature neonates, but decreased integration and segregation even at term-equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth.Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting-state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at-term (n = 332) and preterm (n = 115) neonates at term-equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow-up for some preterm participants, we characterized the developmental trajectories for preterm and at-term neonates, for this purpose linear, quadratic, and log-linear mixed models were constructed with gestational age at scan as an independent fixed-effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term-equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non-linear developmental trajectories for premature neonates, but decreased integration and segregation even at term-equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth. Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting-state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at-term (n = 332) and preterm (n = 115) neonates at term-equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow-up for some preterm participants, we characterized the developmental trajectories for preterm and at-term neonates, for this purpose linear, quadratic, and log-linear mixed models were constructed with gestational age at scan as an independent fixed-effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term-equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non-linear developmental trajectories for premature neonates, but decreased integration and segregation even at term-equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth. ABSTRACT Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident. Resting‐state functional neuroimaging of naturally sleeping babies has shown altered connectivity patterns, but there is limited evidence on the developmental trajectories of functional organization in preterm neonates. By using a large dataset from the developing Human Connectome Project, we explored the differences in graph theory properties between at‐term (n = 332) and preterm (n = 115) neonates at term‐equivalent age, considering the age subgroups proposed by the World Health Organization for premature birth. Leveraging the longitudinal follow‐up for some preterm participants, we characterized the developmental trajectories for preterm and at‐term neonates, for this purpose linear, quadratic, and log‐linear mixed models were constructed with gestational age at scan as an independent fixed‐effect variable and random effects were added for the intercept and subject ID. Significance was defined at p < 0.05, and the model with the lowest Akaike Information Criterion (AIC) was selected as the best model. We found significant differences between groups in connectivity strength, clustering coefficient, characteristic path length and global efficiency. Specifically, at term‐equivalent ages, higher connectivity, clustering coefficient and efficiency are identified for neonates born at later postmenstrual ages. Similarly, the characteristic path length showed the inverse pattern. These results were consistent for a variety of connectivity thresholds at both the global (whole brain) and local level (brain regions). The brain regions with the greatest differences between groups include primary sensory and motor regions and the precuneus which may relate to the risk factors for sensorimotor and behavioral deficits associated with premature birth. Our results also show non‐linear developmental trajectories for premature neonates, but decreased integration and segregation even at term‐equivalent age. Overall, our results confirm altered functional connectivity, integration and segregation properties of the premature brain despite showing rapid maturation after birth. Our results show nonlinear developmental trajectories for different measures of graph theory in preterm infants, but decreased integration and segregation even at term‐equivalent age. |
| Author | López‐Guerrero, N. Alcauter, Sarael |
| AuthorAffiliation | 1 Instituto de Neurobiología Universidad Nacional Autónoma de México Querétaro Mexico |
| AuthorAffiliation_xml | – name: 1 Instituto de Neurobiología Universidad Nacional Autónoma de México Querétaro Mexico |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39815687$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2025 The Author(s). published by Wiley Periodicals LLC. 2025 The Author(s). Human Brain Mapping published by Wiley Periodicals LLC. 2025. This work is published under http://creativecommons.org/licenses/by/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| Keywords | preterm development neonates graph theory brain network |
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| License | Attribution 2025 The Author(s). Human Brain Mapping published by Wiley Periodicals LLC. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. cc-by |
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| Notes | This work was supported by Consejo Nacional de Humanidades, Ciencias y Tecnologías, México (823584) to Nelsiyamid López‐Guerrero, Universidad Nacional Autónoma de México (Programa UNAM‐PAPIIT IN208622) to Sarael Alcauter and European Research Council under the European Union Seventh Framework Programme (FP/2007‐2013)/ERC Grant Agreement no. [319456]. Funding ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Funding: This work was supported by Consejo Nacional de Humanidades, Ciencias y Tecnologías, México (823584) to Nelsiyamid López‐Guerrero, Universidad Nacional Autónoma de México (Programa UNAM‐PAPIIT IN208622) to Sarael Alcauter and European Research Council under the European Union Seventh Framework Programme (FP/2007‐2013)/ERC Grant Agreement no. [319456]. |
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| Snippet | ABSTRACT
Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are... Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are evident.... ABSTRACT Premature infants, born before 37 weeks of gestation can have alterations in neurodevelopment and cognition, even when no anatomical lesions are... |
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| SubjectTerms | Age Brain Brain - diagnostic imaging Brain - growth & development Brain - physiology brain network Child Development - physiology Clustering Cognition Connectome Cortex (parietal) Datasets development Equivalence Female Functional morphology Gestational Age Graph theory Humans Infant, Newborn Infant, Premature - growth & development Infant, Premature - physiology Longitudinal Studies Magnetic Resonance Imaging Male Medical imaging Neonates Nerve Net - diagnostic imaging Nerve Net - growth & development Nerve Net - physiology Neural networks Neural Pathways - diagnostic imaging Neural Pathways - growth & development Neural Pathways - physiology Neurodevelopment Neuroimaging Newborn babies Premature babies Premature birth preterm Risk factors Sensorimotor integration Sensory evaluation Sensory integration Subgroups |
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| Title | Developmental Trajectories and Differences in Functional Brain Network Properties of Preterm and At‐Term Neonates |
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