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Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex

Prematurity is among the leading risks for poor neurocognitive outcomes. The brains of preterm infants show alterations in structure and electrical activity, but the underlying circuit mechanisms are unclear. To address this, we performed a cross-species study of the electrophysiological activity in...

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Autores principales: Witteveen, Isabelle F., McCoy, Emily, Holsworth, Troy D., Shen, Catherine Z., Chang, Winnie, Nance, Madelyn G., Belkowitz, Allison R., Dougald, Avery, Puglia, Meghan H., Ribic, Adema
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10225509/
https://www.ncbi.nlm.nih.gov/pubmed/37255843
http://dx.doi.org/10.3389/fnint.2023.1149159
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author Witteveen, Isabelle F.
McCoy, Emily
Holsworth, Troy D.
Shen, Catherine Z.
Chang, Winnie
Nance, Madelyn G.
Belkowitz, Allison R.
Dougald, Avery
Puglia, Meghan H.
Ribic, Adema
author_facet Witteveen, Isabelle F.
McCoy, Emily
Holsworth, Troy D.
Shen, Catherine Z.
Chang, Winnie
Nance, Madelyn G.
Belkowitz, Allison R.
Dougald, Avery
Puglia, Meghan H.
Ribic, Adema
author_sort Witteveen, Isabelle F.
collection PubMed
description Prematurity is among the leading risks for poor neurocognitive outcomes. The brains of preterm infants show alterations in structure and electrical activity, but the underlying circuit mechanisms are unclear. To address this, we performed a cross-species study of the electrophysiological activity in the visual cortices of prematurely born infants and mice. Using electroencephalography (EEG) in a sample of healthy preterm (N = 29) and term (N = 28) infants, we found that the maturation of the aperiodic EEG component was accelerated in the preterm cohort, with a significantly flatter 1/f slope when compared to the term infants. The flatter slope was a result of decreased spectral power in the theta and alpha bands and was correlated with the degree of prematurity. To determine the circuit and cellular changes that potentially mediate the changes in 1/f slope after preterm birth, we used in vivo electrophysiology in preterm mice and found that, similar to infants, preterm birth results in a flattened 1/f slope. We analyzed neuronal activity in the visual cortex of preterm (N = 6) and term (N = 9) mice and found suppressed spontaneous firing of neurons. Using immunohistochemistry, we further found an accelerated maturation of inhibitory circuits. In both preterm mice and infants, the functional maturation of the cortex was accelerated, underscoring birth as a critical checkpoint in cortical maturation. Our study points to a potential mechanism of preterm birth-related changes in resting neural activity, highlighting the utility of a cross-species approach in studying the neural circuit mechanisms of preterm birth-related neurodevelopmental conditions.
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spelling pubmed-102255092023-05-30 Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex Witteveen, Isabelle F. McCoy, Emily Holsworth, Troy D. Shen, Catherine Z. Chang, Winnie Nance, Madelyn G. Belkowitz, Allison R. Dougald, Avery Puglia, Meghan H. Ribic, Adema Front Integr Neurosci Neuroscience Prematurity is among the leading risks for poor neurocognitive outcomes. The brains of preterm infants show alterations in structure and electrical activity, but the underlying circuit mechanisms are unclear. To address this, we performed a cross-species study of the electrophysiological activity in the visual cortices of prematurely born infants and mice. Using electroencephalography (EEG) in a sample of healthy preterm (N = 29) and term (N = 28) infants, we found that the maturation of the aperiodic EEG component was accelerated in the preterm cohort, with a significantly flatter 1/f slope when compared to the term infants. The flatter slope was a result of decreased spectral power in the theta and alpha bands and was correlated with the degree of prematurity. To determine the circuit and cellular changes that potentially mediate the changes in 1/f slope after preterm birth, we used in vivo electrophysiology in preterm mice and found that, similar to infants, preterm birth results in a flattened 1/f slope. We analyzed neuronal activity in the visual cortex of preterm (N = 6) and term (N = 9) mice and found suppressed spontaneous firing of neurons. Using immunohistochemistry, we further found an accelerated maturation of inhibitory circuits. In both preterm mice and infants, the functional maturation of the cortex was accelerated, underscoring birth as a critical checkpoint in cortical maturation. Our study points to a potential mechanism of preterm birth-related changes in resting neural activity, highlighting the utility of a cross-species approach in studying the neural circuit mechanisms of preterm birth-related neurodevelopmental conditions. Frontiers Media S.A. 2023-05-15 /pmc/articles/PMC10225509/ /pubmed/37255843 http://dx.doi.org/10.3389/fnint.2023.1149159 Text en Copyright © 2023 Witteveen, McCoy, Holsworth, Shen, Chang, Nance, Belkowitz, Dougald, Puglia and Ribic. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Witteveen, Isabelle F.
McCoy, Emily
Holsworth, Troy D.
Shen, Catherine Z.
Chang, Winnie
Nance, Madelyn G.
Belkowitz, Allison R.
Dougald, Avery
Puglia, Meghan H.
Ribic, Adema
Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex
title Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex
title_full Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex
title_fullStr Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex
title_full_unstemmed Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex
title_short Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex
title_sort preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10225509/
https://www.ncbi.nlm.nih.gov/pubmed/37255843
http://dx.doi.org/10.3389/fnint.2023.1149159
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