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Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates

Altered resting state functional connectivity (FC) involving the anterior insula (aINS), a key node in the salience network, has been reported consistently in autism. Here we examined, for the first time, FC between the aINS and the whole brain in a sample of full-term, postmenstrual age (PMA) match...

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Autores principales: Scheinost, Dustin, Chang, Joseph, Lacadie, Cheryl, Brennan-Wydra, Emma, Foster, Rachel, Boxberger, Alexandra, Macari, Suzanne, Vernetti, Angelina, Constable, R. Todd, Ment, Laura R., Chawarska, Katarzyna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9517994/
https://www.ncbi.nlm.nih.gov/pubmed/36171268
http://dx.doi.org/10.1038/s41598-022-20617-6
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author Scheinost, Dustin
Chang, Joseph
Lacadie, Cheryl
Brennan-Wydra, Emma
Foster, Rachel
Boxberger, Alexandra
Macari, Suzanne
Vernetti, Angelina
Constable, R. Todd
Ment, Laura R.
Chawarska, Katarzyna
author_facet Scheinost, Dustin
Chang, Joseph
Lacadie, Cheryl
Brennan-Wydra, Emma
Foster, Rachel
Boxberger, Alexandra
Macari, Suzanne
Vernetti, Angelina
Constable, R. Todd
Ment, Laura R.
Chawarska, Katarzyna
author_sort Scheinost, Dustin
collection PubMed
description Altered resting state functional connectivity (FC) involving the anterior insula (aINS), a key node in the salience network, has been reported consistently in autism. Here we examined, for the first time, FC between the aINS and the whole brain in a sample of full-term, postmenstrual age (PMA) matched neonates (mean 44.0 weeks, SD = 1.5) who due to family history have high likelihood (HL) for developing autism (n = 12) and in controls (n = 41) without family history of autism (low likelihood, LL). Behaviors associated with autism were evaluated between 12 and 18 months (M = 17.3 months, SD = 2.5) in a subsample (25/53) of participants using the First Year Inventory (FYI). Compared to LL controls, HL neonates showed hypoconnectivity between left aINS and left amygdala. Lower connectivity between the two nodes was associated with higher FYI risk scores in the social domain (r(25) = −0.561, p = .003) and this association remained robust when maternal mental health factors were considered. Considering that a subsample of LL participants (n = 14/41) underwent brain imaging during the fetal period at PMA 31 and 34 weeks, in an exploratory analysis, we evaluated prospectively development of the LaINS-Lamy connectivity and found that the two areas strongly coactivate throughout the third trimester of pregnancy. The study identifies left lateralized anterior insula—amygdala connectivity as a potential target of further investigation into neural circuitry that enhances likelihood of future onset of social behaviors associated with autism during neonatal and potentially prenatal periods.
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spelling pubmed-95179942022-09-29 Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates Scheinost, Dustin Chang, Joseph Lacadie, Cheryl Brennan-Wydra, Emma Foster, Rachel Boxberger, Alexandra Macari, Suzanne Vernetti, Angelina Constable, R. Todd Ment, Laura R. Chawarska, Katarzyna Sci Rep Article Altered resting state functional connectivity (FC) involving the anterior insula (aINS), a key node in the salience network, has been reported consistently in autism. Here we examined, for the first time, FC between the aINS and the whole brain in a sample of full-term, postmenstrual age (PMA) matched neonates (mean 44.0 weeks, SD = 1.5) who due to family history have high likelihood (HL) for developing autism (n = 12) and in controls (n = 41) without family history of autism (low likelihood, LL). Behaviors associated with autism were evaluated between 12 and 18 months (M = 17.3 months, SD = 2.5) in a subsample (25/53) of participants using the First Year Inventory (FYI). Compared to LL controls, HL neonates showed hypoconnectivity between left aINS and left amygdala. Lower connectivity between the two nodes was associated with higher FYI risk scores in the social domain (r(25) = −0.561, p = .003) and this association remained robust when maternal mental health factors were considered. Considering that a subsample of LL participants (n = 14/41) underwent brain imaging during the fetal period at PMA 31 and 34 weeks, in an exploratory analysis, we evaluated prospectively development of the LaINS-Lamy connectivity and found that the two areas strongly coactivate throughout the third trimester of pregnancy. The study identifies left lateralized anterior insula—amygdala connectivity as a potential target of further investigation into neural circuitry that enhances likelihood of future onset of social behaviors associated with autism during neonatal and potentially prenatal periods. Nature Publishing Group UK 2022-09-28 /pmc/articles/PMC9517994/ /pubmed/36171268 http://dx.doi.org/10.1038/s41598-022-20617-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Scheinost, Dustin
Chang, Joseph
Lacadie, Cheryl
Brennan-Wydra, Emma
Foster, Rachel
Boxberger, Alexandra
Macari, Suzanne
Vernetti, Angelina
Constable, R. Todd
Ment, Laura R.
Chawarska, Katarzyna
Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates
title Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates
title_full Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates
title_fullStr Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates
title_full_unstemmed Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates
title_short Hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates
title_sort hypoconnectivity between anterior insula and amygdala associates with future vulnerabilities in social development in a neurodiverse sample of neonates
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9517994/
https://www.ncbi.nlm.nih.gov/pubmed/36171268
http://dx.doi.org/10.1038/s41598-022-20617-6
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