Corticolimbic Connectivity Mediates the Relationship Between Pubertal Timing and Mental Health Problems

Overview

Journal Psychol Med

Publisher Cambridge University Press

Specialty Psychology

Date 2023 Jun 2

PMID 37264939

Authors

Nandita Vijayakumar

Sarah Whittle

Timothy J Silk

Affiliations

Soon will be listed here.

Abstract

Background: Undergoing puberty ahead of peers ('earlier pubertal timing') is an important risk factor for mental health problems during early adolescence. The current study examined pathways between pubertal timing and mental health via connectivity of neural systems implicated in emotional reactivity and regulation (specifically corticolimbic connections) in 9- to 14-year-olds.

Method: Research questions were examined in the Adolescent Brain Cognitive Development (ABCD) Study, a large population representative sample in the United States. Linear mixed models examined associations between pubertal timing and resting-state corticolimbic connectivity. Significant connections were examined as potential mediators of the relationship between pubertal timing and mental health (withdrawn depressed and rule-breaking) problems. Exploratory analyses interrogated whether the family environment moderated neural risk patterns in those undergoing puberty earlier than their peers.

Results: Earlier pubertal timing was related to decreased connectivity between limbic structures (bilateral amygdala and right hippocampus) and the cingulo-opercular network, left amygdala and somatomotor (mouth) network, as well as between the left hippocampus and ventral attention network and visual network. Corticolimbic connections also mediated the relationship between earlier pubertal timing and increased withdrawn depressed problems (but not rule-breaking problems). Finally, parental acceptance buffered against connectivity patterns that were implicated in withdrawn depressed problems in those undergoing puberty earlier than their peers.

Conclusion: Findings highlight the role of decreased corticolimbic connectivity in mediating pathways between earlier pubertal timing and withdrawn depressed problems, and we present preliminary evidence that the family environment may buffer against these neural risk patterns during early adolescence.

Citing Articles

Pubertal timing mediates the association between threat adversity and psychopathology.

Shaul M, Whittle S, Silk T, Vijayakumar N Psychol Med. 2024; :1-11.

PMID: 39324385 PMC: 11496226. DOI: 10.1017/S003329172400179X.

References

Aggleton J, Burton M, Passingham R . Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res. 1980; 190(2):347-68. DOI: 10.1016/0006-8993(80)90279-6. View

Cullen K, Westlund M, Klimes-Dougan B, Mueller B, Houri A, Eberly L . Abnormal amygdala resting-state functional connectivity in adolescent depression. JAMA Psychiatry. 2014; 71(10):1138-47. PMC: 4378862. DOI: 10.1001/jamapsychiatry.2014.1087. View

Piekarski D, Johnson C, Boivin J, Thomas A, Lin W, Delevich K . Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?. Brain Res. 2016; 1654(Pt B):123-144. PMC: 5283387. DOI: 10.1016/j.brainres.2016.08.042. View

Shulman E, Smith A, Silva K, Icenogle G, Duell N, Chein J . The dual systems model: Review, reappraisal, and reaffirmation. Dev Cogn Neurosci. 2016; 17:103-17. PMC: 6990093. DOI: 10.1016/j.dcn.2015.12.010. View

Vijayakumar N, Whittle S . A systematic review into the role of pubertal timing and the social environment in adolescent mental health problems. Clin Psychol Rev. 2023; 102:102282. DOI: 10.1016/j.cpr.2023.102282. View

Cressman V, Balaban J, Steinfeld S, Shemyakin A, Graham P, Parisot N . Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat. J Comp Neurol. 2010; 518(14):2693-709. PMC: 3377974. DOI: 10.1002/cne.22359. View

Pannekoek J, van der Werff S, Meens P, van den Bulk B, Jolles D, Veer I . Aberrant resting-state functional connectivity in limbic and salience networks in treatment--naïve clinically depressed adolescents. J Child Psychol Psychiatry. 2014; 55(12):1317-27. DOI: 10.1111/jcpp.12266. View

Cooney R, Joormann J, Eugene F, Dennis E, Gotlib I . Neural correlates of rumination in depression. Cogn Affect Behav Neurosci. 2010; 10(4):470-8. PMC: 4476645. DOI: 10.3758/CABN.10.4.470. View

Ernst M, Benson B, Artiges E, Gorka A, Lemaitre H, Lago T . Pubertal maturation and sex effects on the default-mode network connectivity implicated in mood dysregulation. Transl Psychiatry. 2019; 9(1):103. PMC: 6389927. DOI: 10.1038/s41398-019-0433-6. View

10.

Wu F, Tu Z, Sun J, Geng H, Zhou Y, Jiang X . Abnormal Functional and Structural Connectivity of Amygdala-Prefrontal Circuit in First-Episode Adolescent Depression: A Combined fMRI and DTI Study. Front Psychiatry. 2020; 10:983. PMC: 7013238. DOI: 10.3389/fpsyt.2019.00983. View

11.

Milner T, Thompson L, Wang G, Kievits J, Martin E, Zhou P . Distribution of estrogen receptor β containing cells in the brains of bacterial artificial chromosome transgenic mice. Brain Res. 2010; 1351:74-96. PMC: 2926254. DOI: 10.1016/j.brainres.2010.06.038. View

12.

Wierenga L, Bos M, Schreuders E, Vd Kamp F, Peper J, Tamnes C . Unraveling age, puberty and testosterone effects on subcortical brain development across adolescence. Psychoneuroendocrinology. 2018; 91:105-114. DOI: 10.1016/j.psyneuen.2018.02.034. View

13.

Barbosa C, Simmons J, Vijayakumar N, Dudgeon P, Patton G, Mundy L . Interaction Between Parenting Styles and Adrenarcheal Timing Associated With Affective Brain Function in Late Childhood. J Am Acad Child Adolesc Psychiatry. 2018; 57(9):678-686.e4. DOI: 10.1016/j.jaac.2018.05.016. View

14.

Pozzi E, Vijayakumar N, Byrne M, Bray K, Seal M, Richmond S . Maternal parenting behavior and functional connectivity development in children: A longitudinal fMRI study. Dev Cogn Neurosci. 2021; 48:100946. PMC: 8039548. DOI: 10.1016/j.dcn.2021.100946. View

15.

Thijssen S, Collins P, Weiss H, Luciana M . The longitudinal association between externalizing behavior and frontoamygdalar resting-state functional connectivity in late adolescence and young adulthood. J Child Psychol Psychiatry. 2020; 62(7):857-867. PMC: 8359311. DOI: 10.1111/jcpp.13330. View

16.

van Duijvenvoorde A, Westhoff B, de Vos F, Wierenga L, Crone E . A three-wave longitudinal study of subcortical-cortical resting-state connectivity in adolescence: Testing age- and puberty-related changes. Hum Brain Mapp. 2019; 40(13):3769-3783. PMC: 6767490. DOI: 10.1002/hbm.24630. View

17.

Clark D, Fisher C, Bookheimer S, Brown S, Evans J, Hopfer C . Biomedical ethics and clinical oversight in multisite observational neuroimaging studies with children and adolescents: The ABCD experience. Dev Cogn Neurosci. 2017; 32:143-154. PMC: 5745294. DOI: 10.1016/j.dcn.2017.06.005. View

18.

Cunningham M, Bhattacharyya S, Benes F . Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J Comp Neurol. 2002; 453(2):116-30. DOI: 10.1002/cne.10376. View

19.

Thijssen S, Collins P, Luciana M . Pubertal development mediates the association between family environment and brain structure and function in childhood. Dev Psychopathol. 2019; 32(2):687-702. PMC: 7525116. DOI: 10.1017/S0954579419000580. View

20.

Hanson J, Albert W, Skinner A, Shen S, Dodge K, Lansford J . Resting state coupling between the amygdala and ventromedial prefrontal cortex is related to household income in childhood and indexes future psychological vulnerability to stress. Dev Psychopathol. 2019; 31(3):1053-1066. DOI: 10.1017/S0954579419000592. View