Rewiring the extremely preterm brain: Altered structural connectivity relates to language function

Children born preterm are at increased risk for cognitive impairment, with higher-order functions such as language being especially vulnerable. Previously, we and others have reported increased interhemispheric functional connectivity in children born extremely preterm; the finding appears at odds w...

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Main Authors: Maria E. Barnes-Davis, Brady J. Williamson, Stephanie L. Merhar, Scott K. Holland, Darren S. Kadis
Format: Article
Language:English
Published: Elsevier 2020-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158220300310
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spelling doaj-e5c7c530d2e94ef28c6f9b5f1a5ddfc72020-11-25T03:48:15ZengElsevierNeuroImage: Clinical2213-15822020-01-0125Rewiring the extremely preterm brain: Altered structural connectivity relates to language functionMaria E. Barnes-Davis0Brady J. Williamson1Stephanie L. Merhar2Scott K. Holland3Darren S. Kadis4Perinatal Institute, Cincinnati Children's Hospital Medical Center, United States; Department of Pediatrics, University of Cincinnati College of Medicine, United States; Corresponding author at: Cincinnati Children's Hospital Medical Center, Perinatal Institute, 3333 Burnet Ave, Cincinnati, OH 45229, United States.Department of Psychology, University of Cincinnati, United States; Pediatric Neuroimaging Research Consortium, Cincinnati Children's Hospital Medical Center, United StatesPerinatal Institute, Cincinnati Children's Hospital Medical Center, United States; Department of Pediatrics, University of Cincinnati College of Medicine, United StatesDepartment of Physics, University of Cincinnati, United States; Medpace Imaging Core Laboratory, Medpace Inc., United StatesNeurosciences and Mental Health Research Institute, Hospital for Sick Children, Canada; Department of Physiology, Faculty of Medicine, University of Toronto, CanadaChildren born preterm are at increased risk for cognitive impairment, with higher-order functions such as language being especially vulnerable. Previously, we and others have reported increased interhemispheric functional connectivity in children born extremely preterm; the finding appears at odds with literature showing decreased integrity of the corpus callosum, the primary commissural bundle, in preterm children. We address the apparent discrepancy by obtaining advanced measures of structural connectivity in twelve school-aged children born extremely preterm (<28 weeks) and ten term controls. We hypothesize increased extracallosal structural connectivity might support the functional hyperconnectivity we had previously observed. Participants were aged four to six years at time of study and groups did not differ in age, sex, race, ethnicity, or socioeconomic status. Whole-brain and language-network-specific (functionally-constrained) connectometry analyses were performed. At the whole-brain level, preterm children had decreased connectivity in the corpus callosum and increased connectivity in the cerebellum versus controls. Functionally-constrained analyses revealed significantly increased extracallosal connectivity between bilateral temporal regions in preterm children (FDRq <0.05). Connectivity within these extracallosal pathways was positively correlated with performance on standardized language assessments in children born preterm (FDRq <0.001), but unrelated to performance in controls. This is the first study to identify anatomical substrates for increased interhemispheric functional connectivity in children born preterm; increased reliance on an extracallosal pathway may represent a biomarker for resiliency following extremely preterm birth. Keywords: Prematurity, Language, Diffusion, Connectivity, Developmenthttp://www.sciencedirect.com/science/article/pii/S2213158220300310
collection DOAJ
language English
format Article
sources DOAJ
author Maria E. Barnes-Davis
Brady J. Williamson
Stephanie L. Merhar
Scott K. Holland
Darren S. Kadis
spellingShingle Maria E. Barnes-Davis
Brady J. Williamson
Stephanie L. Merhar
Scott K. Holland
Darren S. Kadis
Rewiring the extremely preterm brain: Altered structural connectivity relates to language function
NeuroImage: Clinical
author_facet Maria E. Barnes-Davis
Brady J. Williamson
Stephanie L. Merhar
Scott K. Holland
Darren S. Kadis
author_sort Maria E. Barnes-Davis
title Rewiring the extremely preterm brain: Altered structural connectivity relates to language function
title_short Rewiring the extremely preterm brain: Altered structural connectivity relates to language function
title_full Rewiring the extremely preterm brain: Altered structural connectivity relates to language function
title_fullStr Rewiring the extremely preterm brain: Altered structural connectivity relates to language function
title_full_unstemmed Rewiring the extremely preterm brain: Altered structural connectivity relates to language function
title_sort rewiring the extremely preterm brain: altered structural connectivity relates to language function
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2020-01-01
description Children born preterm are at increased risk for cognitive impairment, with higher-order functions such as language being especially vulnerable. Previously, we and others have reported increased interhemispheric functional connectivity in children born extremely preterm; the finding appears at odds with literature showing decreased integrity of the corpus callosum, the primary commissural bundle, in preterm children. We address the apparent discrepancy by obtaining advanced measures of structural connectivity in twelve school-aged children born extremely preterm (<28 weeks) and ten term controls. We hypothesize increased extracallosal structural connectivity might support the functional hyperconnectivity we had previously observed. Participants were aged four to six years at time of study and groups did not differ in age, sex, race, ethnicity, or socioeconomic status. Whole-brain and language-network-specific (functionally-constrained) connectometry analyses were performed. At the whole-brain level, preterm children had decreased connectivity in the corpus callosum and increased connectivity in the cerebellum versus controls. Functionally-constrained analyses revealed significantly increased extracallosal connectivity between bilateral temporal regions in preterm children (FDRq <0.05). Connectivity within these extracallosal pathways was positively correlated with performance on standardized language assessments in children born preterm (FDRq <0.001), but unrelated to performance in controls. This is the first study to identify anatomical substrates for increased interhemispheric functional connectivity in children born preterm; increased reliance on an extracallosal pathway may represent a biomarker for resiliency following extremely preterm birth. Keywords: Prematurity, Language, Diffusion, Connectivity, Development
url http://www.sciencedirect.com/science/article/pii/S2213158220300310
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