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

Szczupak, Diego and Yen, Cecil C. and Liu, Cirong and Tian, Xiaoguang and Lent, Roberto and Tovar-Moll, Fernanda and Silva, Afonso C. (2020) Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum. Frontiers in Neural Circuits, 14 . Art. No. 612595. ISSN 1662-5110. PMCID PMC7779638. doi:10.3389/fncir.2020.612595.

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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.

Item Type:Article
Related URLs:
URLURL TypeDescription CentralArticle
https://www.irc5.orgRelated ItemInternational Research Consortium for the Corpus Callosum and Cerebral Connectivity
Szczupak, Diego0000-0003-0818-9613
Yen, Cecil C.0000-0002-1519-9791
Liu, Cirong0000-0002-7986-4615
Lent, Roberto0000-0002-8989-4009
Tovar-Moll, Fernanda0000-0002-0292-5985
Silva, Afonso C.0000-0002-6105-7567
Other Contributors:
ContributionOther Contributors NameIdentifierPersonID (may be blank)
CollaboratorPaul, Lynn K.Paul-Lynn-KUNSPECIFIED
Additional Information:© 2020 Szczupak, Yen, Liu, Tian, Lent, Tovar-Moll and Silva. 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. Received: 30 September 2020; Accepted: 24 November 2020; Published: 21 December 2020. We would like to thank Ivanei Bramatti, Marina Carneiro, Fernanda Meireles, and Xianfeng (Lisa) Zhang for technical support. We also thank the members and affiliates of the International Research Consortium for the Corpus Callosum and Cerebral Connectivity (IRC5, for constructive discussions on the subject matter of this publication. Funding: This work was supported by the PA Department of Health SAP #4100083102 to ACS. The research was also supported by the Research Support Foundation of the State of Rio de Janeiro (FAPERJ), by the National Council for Scientific and Technological Development (CNPq), as well as by intramural grants from D’Or Institute for Research and Education (IDOR). This research was supported (in part) by the Intramural Research Program of the NIH, NINDS (grant ZIANS003041 to ACS). Ethics Statement: The animal study was reviewed and approved by the Animal Care and Use Committee of the National Institute of Neurological Disorders and Stroke. The studies involving human participants were reviewed and approved by the Ethics committee of the D’Or Institute for Research and Education (Rio de Janeiro, Brazil). Written informed consent to participate in this study was provided by the participants’ legal guardian/next of kin. Written informed consent was obtained from the individual(s), and minor(s)’ legal guardian/next of kin, for the publication of any potentially identifiable images or data included in this article. Author Contributions: DS, CY, CL, and XT acquired animal data. DS and ACS designed experiments and analyses. FT-M provided human CCD data. DS, ACS, FT-M, and RL wrote the manuscript, and all authors contributed with the manuscript revision. All authors contributed to the article and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Funding AgencyGrant Number
Pennsylvania Department of Health4100083102
Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ)UNSPECIFIED
Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)UNSPECIFIED
D’Or Institute for Research and Education (IDOR)UNSPECIFIED
Subject Keywords:cingulate cortex, corpus callosum, dynamic functional connectivity, dysgenesis of the corpus callosum, marmosets, non-human primates, quasi-periodic patterns, sensory cortex
PubMed Central ID:PMC7779638
Record Number:CaltechAUTHORS:20210302-105436724
Persistent URL:
Official Citation:Szczupak D, Yen CC, Liu C, Tian X, Lent R, Tovar-Moll F and Silva AC (2020) Dynamic Interhemispheric Desynchronization in Marmosets and Humans With Disorders of the Corpus Callosum. Front. Neural Circuits 14:612595. doi: 10.3389/fncir.2020.612595
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108270
Deposited By: Tony Diaz
Deposited On:02 Mar 2021 19:07
Last Modified:16 Nov 2021 19:10

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