Cargando…

Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics

The transition from childhood to adolescence is associated with an influx of sex hormones, which not only facilitates physical and behavioral changes, but also dramatic changes in neural circuitry. While previous work has shown that pubertal hormones modulate structural and functional brain developm...

Descripción completa

Detalles Bibliográficos
Autores principales: Picci, Giorgia, Ott, Lauren R., Penhale, Samantha H., Taylor, Brittany K., Johnson, Hallie J., Willett, Madelyn P., Okelberry, Hannah J., Wang, Yu‐Ping, Calhoun, Vince D., Stephen, Julia M., Wilson, Tony W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619376/
https://www.ncbi.nlm.nih.gov/pubmed/37811842
http://dx.doi.org/10.1002/hbm.26496
_version_ 1785129975595139072
author Picci, Giorgia
Ott, Lauren R.
Penhale, Samantha H.
Taylor, Brittany K.
Johnson, Hallie J.
Willett, Madelyn P.
Okelberry, Hannah J.
Wang, Yu‐Ping
Calhoun, Vince D.
Stephen, Julia M.
Wilson, Tony W.
author_facet Picci, Giorgia
Ott, Lauren R.
Penhale, Samantha H.
Taylor, Brittany K.
Johnson, Hallie J.
Willett, Madelyn P.
Okelberry, Hannah J.
Wang, Yu‐Ping
Calhoun, Vince D.
Stephen, Julia M.
Wilson, Tony W.
author_sort Picci, Giorgia
collection PubMed
description The transition from childhood to adolescence is associated with an influx of sex hormones, which not only facilitates physical and behavioral changes, but also dramatic changes in neural circuitry. While previous work has shown that pubertal hormones modulate structural and functional brain development, few of these studies have focused on the impact that such hormones have on spontaneous cortical activity, and whether these effects are modulated by sex during this critical developmental window. Herein, we examined the effect of endogenous testosterone on spontaneous cortical activity in 71 typically‐developing youth (ages 10–17 years; 32 male). Participants completed a resting‐state magnetoencephalographic (MEG) recording, structural MRI, and provided a saliva sample for hormone analysis. MEG data were source‐reconstructed and the power within five canonical frequency bands (delta, theta, alpha, beta, and gamma) was computed. The resulting power spectral density maps were analyzed via vertex‐wise ANCOVAs to identify spatially specific effects of testosterone and sex by testosterone interactions, while covarying out age. We found robust sex differences in the modulatory effects of testosterone on spontaneous delta, beta, and gamma activity. These interactions were largely confined to frontal cortices and exhibited a stark switch in the directionality of the correlation from the low (delta) to high frequencies (beta/gamma). For example, in the delta band, greater testosterone related to lower relative power in prefrontal cortices in boys, while the reverse pattern was found for girls. These data suggest testosterone levels are uniquely related to the development of spontaneous cortical dynamics during adolescence, and such levels are associated with different developmental patterns in males and females within regions implicated in executive functioning.
format Online
Article
Text
id pubmed-10619376
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher John Wiley & Sons, Inc.
record_format MEDLINE/PubMed
spelling pubmed-106193762023-11-02 Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics Picci, Giorgia Ott, Lauren R. Penhale, Samantha H. Taylor, Brittany K. Johnson, Hallie J. Willett, Madelyn P. Okelberry, Hannah J. Wang, Yu‐Ping Calhoun, Vince D. Stephen, Julia M. Wilson, Tony W. Hum Brain Mapp Research Articles The transition from childhood to adolescence is associated with an influx of sex hormones, which not only facilitates physical and behavioral changes, but also dramatic changes in neural circuitry. While previous work has shown that pubertal hormones modulate structural and functional brain development, few of these studies have focused on the impact that such hormones have on spontaneous cortical activity, and whether these effects are modulated by sex during this critical developmental window. Herein, we examined the effect of endogenous testosterone on spontaneous cortical activity in 71 typically‐developing youth (ages 10–17 years; 32 male). Participants completed a resting‐state magnetoencephalographic (MEG) recording, structural MRI, and provided a saliva sample for hormone analysis. MEG data were source‐reconstructed and the power within five canonical frequency bands (delta, theta, alpha, beta, and gamma) was computed. The resulting power spectral density maps were analyzed via vertex‐wise ANCOVAs to identify spatially specific effects of testosterone and sex by testosterone interactions, while covarying out age. We found robust sex differences in the modulatory effects of testosterone on spontaneous delta, beta, and gamma activity. These interactions were largely confined to frontal cortices and exhibited a stark switch in the directionality of the correlation from the low (delta) to high frequencies (beta/gamma). For example, in the delta band, greater testosterone related to lower relative power in prefrontal cortices in boys, while the reverse pattern was found for girls. These data suggest testosterone levels are uniquely related to the development of spontaneous cortical dynamics during adolescence, and such levels are associated with different developmental patterns in males and females within regions implicated in executive functioning. John Wiley & Sons, Inc. 2023-10-09 /pmc/articles/PMC10619376/ /pubmed/37811842 http://dx.doi.org/10.1002/hbm.26496 Text en © 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Research Articles
Picci, Giorgia
Ott, Lauren R.
Penhale, Samantha H.
Taylor, Brittany K.
Johnson, Hallie J.
Willett, Madelyn P.
Okelberry, Hannah J.
Wang, Yu‐Ping
Calhoun, Vince D.
Stephen, Julia M.
Wilson, Tony W.
Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics
title Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics
title_full Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics
title_fullStr Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics
title_full_unstemmed Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics
title_short Developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics
title_sort developmental changes in endogenous testosterone have sexually‐dimorphic effects on spontaneous cortical dynamics
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619376/
https://www.ncbi.nlm.nih.gov/pubmed/37811842
http://dx.doi.org/10.1002/hbm.26496
work_keys_str_mv AT piccigiorgia developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT ottlaurenr developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT penhalesamanthah developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT taylorbrittanyk developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT johnsonhalliej developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT willettmadelynp developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT okelberryhannahj developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT wangyuping developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT calhounvinced developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT stephenjuliam developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics
AT wilsontonyw developmentalchangesinendogenoustestosteronehavesexuallydimorphiceffectsonspontaneouscorticaldynamics