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Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum

The corpus callosum, the principal structural avenue for interhemispheric neuronal communication, controls the brain’s lateralization. Developmental malformations of the corpus callosum (CCD) can lead to learning and intellectual disabilities. Currently, there is no clear explanation for these sympt...

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Autores principales: Szczupak, Diego, Yen, Cecil C., Liu, Cirong, Tian, Xiaoguang, Lent, Roberto, Tovar-Moll, Fernanda, Silva, Afonso C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7779638/
https://www.ncbi.nlm.nih.gov/pubmed/33408615
http://dx.doi.org/10.3389/fncir.2020.612595
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author Szczupak, Diego
Yen, Cecil C.
Liu, Cirong
Tian, Xiaoguang
Lent, Roberto
Tovar-Moll, Fernanda
Silva, Afonso C.
author_facet Szczupak, Diego
Yen, Cecil C.
Liu, Cirong
Tian, Xiaoguang
Lent, Roberto
Tovar-Moll, Fernanda
Silva, Afonso C.
author_sort Szczupak, Diego
collection PubMed
description The corpus callosum, the principal structural avenue for interhemispheric neuronal communication, controls the brain’s lateralization. Developmental malformations of the corpus callosum (CCD) can lead to learning and intellectual disabilities. Currently, there is no clear explanation for these symptoms. Here, we used resting-state functional MRI (rsfMRI) to evaluate the dynamic resting-state functional connectivity (rsFC) in both the cingulate cortex (CG) and the sensory areas (S1, S2, A1) in three marmosets (Callithrix jacchus) with spontaneous CCD. We also performed rsfMRI in 10 CCD human subjects (six hypoplasic and four agenesic). We observed no differences in the strength of rsFC between homotopic CG and sensory areas in both species when comparing them to healthy controls. However, in CCD marmosets, we found lower strength of quasi-periodic patterns (QPP) correlation in the posterior interhemispheric sensory areas. We also found a significant lag of interhemispheric communication in the medial CG, suggesting asynchrony between the two hemispheres. Correspondingly, in human subjects, we found that the CG of acallosal subjects had a higher QPP correlation than controls. In comparison, hypoplasic subjects had a lower QPP correlation and a delay of 1.6 s in the sensory regions. These results show that CCD affects the interhemispheric synchrony of both CG and sensory areas and that, in both species, its impact on cortical communication varies along the CC development gradient. Our study shines a light on how CCD misconnects homotopic regions and opens a line of research to explain the causes of the symptoms exhibited by CCD patients and how to mitigate them.
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spelling pubmed-77796382021-01-05 Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum Szczupak, Diego Yen, Cecil C. Liu, Cirong Tian, Xiaoguang Lent, Roberto Tovar-Moll, Fernanda Silva, Afonso C. Front Neural Circuits Neuroscience The corpus callosum, the principal structural avenue for interhemispheric neuronal communication, controls the brain’s lateralization. Developmental malformations of the corpus callosum (CCD) can lead to learning and intellectual disabilities. Currently, there is no clear explanation for these symptoms. Here, we used resting-state functional MRI (rsfMRI) to evaluate the dynamic resting-state functional connectivity (rsFC) in both the cingulate cortex (CG) and the sensory areas (S1, S2, A1) in three marmosets (Callithrix jacchus) with spontaneous CCD. We also performed rsfMRI in 10 CCD human subjects (six hypoplasic and four agenesic). We observed no differences in the strength of rsFC between homotopic CG and sensory areas in both species when comparing them to healthy controls. However, in CCD marmosets, we found lower strength of quasi-periodic patterns (QPP) correlation in the posterior interhemispheric sensory areas. We also found a significant lag of interhemispheric communication in the medial CG, suggesting asynchrony between the two hemispheres. Correspondingly, in human subjects, we found that the CG of acallosal subjects had a higher QPP correlation than controls. In comparison, hypoplasic subjects had a lower QPP correlation and a delay of 1.6 s in the sensory regions. These results show that CCD affects the interhemispheric synchrony of both CG and sensory areas and that, in both species, its impact on cortical communication varies along the CC development gradient. Our study shines a light on how CCD misconnects homotopic regions and opens a line of research to explain the causes of the symptoms exhibited by CCD patients and how to mitigate them. Frontiers Media S.A. 2020-12-21 /pmc/articles/PMC7779638/ /pubmed/33408615 http://dx.doi.org/10.3389/fncir.2020.612595 Text en Copyright © 2020 Szczupak, Yen, Liu, Tian, Lent, Tovar-Moll and Silva. http://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
Szczupak, Diego
Yen, Cecil C.
Liu, Cirong
Tian, Xiaoguang
Lent, Roberto
Tovar-Moll, Fernanda
Silva, Afonso C.
Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum
title Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum
title_full Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum
title_fullStr Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum
title_full_unstemmed Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum
title_short Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum
title_sort dynamic interhemispheric desynchronization in marmosets and humans with disorders of the corpus callosum
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7779638/
https://www.ncbi.nlm.nih.gov/pubmed/33408615
http://dx.doi.org/10.3389/fncir.2020.612595
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