Sex and age variations in the impact of puberty on cortical thickness and associations with internalizing symptoms and suicidal ideation in early adolescence

Andrea Wiglesworth; Mark B. Fiecas; Meng Xu; Aidan T. Neher; Laura Padilla; Katherine A. Carosella; Donovan J. Roediger; Bryon A. Mueller; Monica Luciana; Bonnie Klimes-Dougan; Kathryn R. Cullen

doi:10.1016/j.dcn.2022.101195

Sex and age variations in the impact of puberty on cortical thickness and associations with internalizing symptoms and suicidal ideation in early adolescence

Andrea Wiglesworth, Mark B. Fiecas, Meng Xu, Aidan T. Neher, Laura Padilla, Katherine A. Carosella, Donovan J. Roediger, Bryon A. Mueller, Monica Luciana, Bonnie Klimes-Dougan, Kathryn R. Cullen

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Purpose: The childhood-to-adolescence transition is a notable period of change including pubertal development, neurodevelopment, and psychopathology onset, that occurs in divergent patterns between sexes. This study examined the effects of sex and puberty on cortical thickness (CT) in children and explored whether CT changes over time related to emergence of psychopathology in early adolescence. Methods: We used longitudinal data (baseline ages 9–10 and Year 2 [Y2] ages 11–12) from the ABCD Study (n = 9985). Linear and penalized function-on-function regressions modeled the impact of puberty, as it interacts with sex, on CT. Focusing on regions that showed sex differences, linear and logistic regressions modeled associations between change in CT and internalizing problems and suicide ideation. Results: We identified significant sex differences in the inverse relation between puberty and CT in fifteen primarily posterior brain regions. Nonlinear pubertal effects across age were identified in the fusiform, isthmus cingulate, paracentral, and precuneus. All effects were stronger for females relative to males during this developmental window. We did not identify associations between CT change and early adolescent clinical outcomes. Conclusion: During this age range, puberty is most strongly associated with regional changes in CT in females, which may have implications for the later emergence of psychopathology.

Original language	English (US)
Article number	101195
Journal	Developmental Cognitive Neuroscience
Volume	59
DOIs	https://doi.org/10.1016/j.dcn.2022.101195
State	Published - Feb 2023

Bibliographical note

Funding Information:
The authors would like to thank the children, adolescents, and family members who participated in the study. This project was supported by NIH grant R01MH122473 (Author K.R.C.). Author A.W. is funded by the National Science Foundation Graduate Research Fellowship Program. Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development (ABCD) Study (https://abcdstudy.org), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study® is supported by the National Institutes of Health and additional federal partners under award numbers U01DA041048, U01DA050989, U01DA051016, U01DA041022, U01DA051018, U01DA051037, U01DA050987, U01DA041174, U01DA041106, U01DA041117, U01DA041028, U01DA041134, U01DA050988, U01DA051039, U01DA041156, U01DA041025, U01DA041120, U01DA051038, U01DA041148, U01DA041093, U01DA041089, U24DA041123, U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners.html. A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortium_members/. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from Data Release Version 4.0. DOIs can be found at http://dx.doi.org/10.15154/1523041.

Funding Information:
The authors would like to thank the children, adolescents, and family members who participated in the study. This project was supported by NIH grant R01MH122473 (Author K.R.C.). Author A.W. is funded by the National Science Foundation Graduate Research Fellowship Program . Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development (ABCD) Study ( https://abcdstudy.org ), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study® is supported by the National Institutes of Health and additional federal partners under award numbers U01DA041048 , U01DA050989 , U01DA051016 , U01DA041022 , U01DA051018 , U01DA051037 , U01DA050987 , U01DA041174 , U01DA041106 , U01DA041117 , U01DA041028 , U01DA041134 , U01DA050988 , U01DA051039 , U01DA041156 , U01DA041025 , U01DA041120 , U01DA051038 , U01DA041148 , U01DA041093 , U01DA041089 , U24DA041123 , U24DA041147 . A full list of supporters is available at https://abcdstudy.org/federal-partners.html . A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortium_members/ . ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from Data Release Version 4.0. DOIs can be found at http://dx.doi.org/10.15154/1523041 .

Publisher Copyright:
© 2023 The Authors

Keywords

Cortical thickness
Developmental psychopathology
Neurodevelopment
Puberty
Sex differences
Suicidal ideation

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.dcn.2022.101195

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Wiglesworth, A., Fiecas, M. B., Xu, M., Neher, A. T., Padilla, L., Carosella, K. A., Roediger, D. J., Mueller, B. A., Luciana, M., Klimes-Dougan, B., & Cullen, K. R. (2023). Sex and age variations in the impact of puberty on cortical thickness and associations with internalizing symptoms and suicidal ideation in early adolescence. Developmental Cognitive Neuroscience, 59, Article 101195. https://doi.org/10.1016/j.dcn.2022.101195

Wiglesworth, A, Fiecas, MB, Xu, M, Neher, AT, Padilla, L, Carosella, KA, Roediger, DJ, Mueller, BA , Luciana, M , Klimes-Dougan, B & Cullen, KR 2023, 'Sex and age variations in the impact of puberty on cortical thickness and associations with internalizing symptoms and suicidal ideation in early adolescence', Developmental Cognitive Neuroscience, vol. 59, 101195. https://doi.org/10.1016/j.dcn.2022.101195

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title = "Sex and age variations in the impact of puberty on cortical thickness and associations with internalizing symptoms and suicidal ideation in early adolescence",

abstract = "Purpose: The childhood-to-adolescence transition is a notable period of change including pubertal development, neurodevelopment, and psychopathology onset, that occurs in divergent patterns between sexes. This study examined the effects of sex and puberty on cortical thickness (CT) in children and explored whether CT changes over time related to emergence of psychopathology in early adolescence. Methods: We used longitudinal data (baseline ages 9–10 and Year 2 [Y2] ages 11–12) from the ABCD Study (n = 9985). Linear and penalized function-on-function regressions modeled the impact of puberty, as it interacts with sex, on CT. Focusing on regions that showed sex differences, linear and logistic regressions modeled associations between change in CT and internalizing problems and suicide ideation. Results: We identified significant sex differences in the inverse relation between puberty and CT in fifteen primarily posterior brain regions. Nonlinear pubertal effects across age were identified in the fusiform, isthmus cingulate, paracentral, and precuneus. All effects were stronger for females relative to males during this developmental window. We did not identify associations between CT change and early adolescent clinical outcomes. Conclusion: During this age range, puberty is most strongly associated with regional changes in CT in females, which may have implications for the later emergence of psychopathology.",

keywords = "Cortical thickness, Developmental psychopathology, Neurodevelopment, Puberty, Sex differences, Suicidal ideation",

author = "Andrea Wiglesworth and Fiecas, {Mark B.} and Meng Xu and Neher, {Aidan T.} and Laura Padilla and Carosella, {Katherine A.} and Roediger, {Donovan J.} and Mueller, {Bryon A.} and Monica Luciana and Bonnie Klimes-Dougan and Cullen, {Kathryn R.}",

note = "Funding Information: The authors would like to thank the children, adolescents, and family members who participated in the study. This project was supported by NIH grant R01MH122473 (Author K.R.C.). Author A.W. is funded by the National Science Foundation Graduate Research Fellowship Program. Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development (ABCD) Study (https://abcdstudy.org), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study{\textregistered} is supported by the National Institutes of Health and additional federal partners under award numbers U01DA041048, U01DA050989, U01DA051016, U01DA041022, U01DA051018, U01DA051037, U01DA050987, U01DA041174, U01DA041106, U01DA041117, U01DA041028, U01DA041134, U01DA050988, U01DA051039, U01DA041156, U01DA041025, U01DA041120, U01DA051038, U01DA041148, U01DA041093, U01DA041089, U24DA041123, U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners.html. A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortium_members/. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from Data Release Version 4.0. DOIs can be found at http://dx.doi.org/10.15154/1523041. Funding Information: The authors would like to thank the children, adolescents, and family members who participated in the study. This project was supported by NIH grant R01MH122473 (Author K.R.C.). Author A.W. is funded by the National Science Foundation Graduate Research Fellowship Program . Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development (ABCD) Study ( https://abcdstudy.org ), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study{\textregistered} is supported by the National Institutes of Health and additional federal partners under award numbers U01DA041048 , U01DA050989 , U01DA051016 , U01DA041022 , U01DA051018 , U01DA051037 , U01DA050987 , U01DA041174 , U01DA041106 , U01DA041117 , U01DA041028 , U01DA041134 , U01DA050988 , U01DA051039 , U01DA041156 , U01DA041025 , U01DA041120 , U01DA051038 , U01DA041148 , U01DA041093 , U01DA041089 , U24DA041123 , U24DA041147 . A full list of supporters is available at https://abcdstudy.org/federal-partners.html . A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortium_members/ . ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from Data Release Version 4.0. DOIs can be found at http://dx.doi.org/10.15154/1523041 . Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2023",

month = feb,

doi = "10.1016/j.dcn.2022.101195",

language = "English (US)",

volume = "59",

journal = "Developmental Cognitive Neuroscience",

issn = "1878-9293",

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T1 - Sex and age variations in the impact of puberty on cortical thickness and associations with internalizing symptoms and suicidal ideation in early adolescence

AU - Wiglesworth, Andrea

AU - Fiecas, Mark B.

AU - Xu, Meng

AU - Neher, Aidan T.

AU - Padilla, Laura

AU - Carosella, Katherine A.

AU - Roediger, Donovan J.

AU - Mueller, Bryon A.

AU - Luciana, Monica

AU - Klimes-Dougan, Bonnie

AU - Cullen, Kathryn R.

N1 - Funding Information: The authors would like to thank the children, adolescents, and family members who participated in the study. This project was supported by NIH grant R01MH122473 (Author K.R.C.). Author A.W. is funded by the National Science Foundation Graduate Research Fellowship Program. Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development (ABCD) Study (https://abcdstudy.org), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study® is supported by the National Institutes of Health and additional federal partners under award numbers U01DA041048, U01DA050989, U01DA051016, U01DA041022, U01DA051018, U01DA051037, U01DA050987, U01DA041174, U01DA041106, U01DA041117, U01DA041028, U01DA041134, U01DA050988, U01DA051039, U01DA041156, U01DA041025, U01DA041120, U01DA051038, U01DA041148, U01DA041093, U01DA041089, U24DA041123, U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners.html. A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortium_members/. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from Data Release Version 4.0. DOIs can be found at http://dx.doi.org/10.15154/1523041. Funding Information: The authors would like to thank the children, adolescents, and family members who participated in the study. This project was supported by NIH grant R01MH122473 (Author K.R.C.). Author A.W. is funded by the National Science Foundation Graduate Research Fellowship Program . Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development (ABCD) Study ( https://abcdstudy.org ), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study® is supported by the National Institutes of Health and additional federal partners under award numbers U01DA041048 , U01DA050989 , U01DA051016 , U01DA041022 , U01DA051018 , U01DA051037 , U01DA050987 , U01DA041174 , U01DA041106 , U01DA041117 , U01DA041028 , U01DA041134 , U01DA050988 , U01DA051039 , U01DA041156 , U01DA041025 , U01DA041120 , U01DA051038 , U01DA041148 , U01DA041093 , U01DA041089 , U24DA041123 , U24DA041147 . A full list of supporters is available at https://abcdstudy.org/federal-partners.html . A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortium_members/ . ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from Data Release Version 4.0. DOIs can be found at http://dx.doi.org/10.15154/1523041 . Publisher Copyright: © 2023 The Authors

PY - 2023/2

Y1 - 2023/2

N2 - Purpose: The childhood-to-adolescence transition is a notable period of change including pubertal development, neurodevelopment, and psychopathology onset, that occurs in divergent patterns between sexes. This study examined the effects of sex and puberty on cortical thickness (CT) in children and explored whether CT changes over time related to emergence of psychopathology in early adolescence. Methods: We used longitudinal data (baseline ages 9–10 and Year 2 [Y2] ages 11–12) from the ABCD Study (n = 9985). Linear and penalized function-on-function regressions modeled the impact of puberty, as it interacts with sex, on CT. Focusing on regions that showed sex differences, linear and logistic regressions modeled associations between change in CT and internalizing problems and suicide ideation. Results: We identified significant sex differences in the inverse relation between puberty and CT in fifteen primarily posterior brain regions. Nonlinear pubertal effects across age were identified in the fusiform, isthmus cingulate, paracentral, and precuneus. All effects were stronger for females relative to males during this developmental window. We did not identify associations between CT change and early adolescent clinical outcomes. Conclusion: During this age range, puberty is most strongly associated with regional changes in CT in females, which may have implications for the later emergence of psychopathology.

AB - Purpose: The childhood-to-adolescence transition is a notable period of change including pubertal development, neurodevelopment, and psychopathology onset, that occurs in divergent patterns between sexes. This study examined the effects of sex and puberty on cortical thickness (CT) in children and explored whether CT changes over time related to emergence of psychopathology in early adolescence. Methods: We used longitudinal data (baseline ages 9–10 and Year 2 [Y2] ages 11–12) from the ABCD Study (n = 9985). Linear and penalized function-on-function regressions modeled the impact of puberty, as it interacts with sex, on CT. Focusing on regions that showed sex differences, linear and logistic regressions modeled associations between change in CT and internalizing problems and suicide ideation. Results: We identified significant sex differences in the inverse relation between puberty and CT in fifteen primarily posterior brain regions. Nonlinear pubertal effects across age were identified in the fusiform, isthmus cingulate, paracentral, and precuneus. All effects were stronger for females relative to males during this developmental window. We did not identify associations between CT change and early adolescent clinical outcomes. Conclusion: During this age range, puberty is most strongly associated with regional changes in CT in females, which may have implications for the later emergence of psychopathology.

KW - Cortical thickness

KW - Developmental psychopathology

KW - Neurodevelopment

KW - Puberty

KW - Sex differences

KW - Suicidal ideation

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Sex and age variations in the impact of puberty on cortical thickness and associations with internalizing symptoms and suicidal ideation in early adolescence

Abstract

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