Early-life and Pubertal Stress Differentially Modulate Grey Matter Development in Human Adolescents

Overview

Journal Sci Rep

Specialty Science

Date 2018 Jun 17

PMID 29907813

Citations 49

Authors

Anna Tyborowska

Inge Volman

Hannah C M Niermann

J Loes Pouwels

Sanny Smeekens

Antonius H N Cillessen

Ivan Toni

Karin Roelofs

Affiliations

Soon will be listed here.

Abstract

Animal and human studies have shown that both early-life traumatic events and ongoing stress episodes affect neurodevelopment, however, it remains unclear whether and how they modulate normative adolescent neuro-maturational trajectories. We characterized effects of early-life (age 0-5) and ongoing stressors (age 14-17) on longitudinal changes (age 14 to17) in grey matter volume (GMV) of healthy adolescents (n = 37). Timing and stressor type were related to differential GMV changes. More personal early-life stressful events were associated with larger developmental reductions in GMV over anterior prefrontal cortex, amygdala and other subcortical regions; whereas ongoing stress from the adolescents' social environment was related to smaller reductions over the orbitofrontal and anterior cingulate cortex. These findings suggest that early-life stress accelerates pubertal development, whereas an adverse adolescent social environment disturbs brain maturation with potential mental health implications: delayed anterior cingulate maturation was associated with more antisocial traits - a juvenile precursor of psychopathy.

Citing Articles

Relationships of eating behaviors with psychopathology, brain maturation and genetic risk for obesity in an adolescent cohort study.

Yu X, Zhang Z, Herle M, Banaschewski T, Barker G, Bokde A Nat Ment Health. 2025; 3(1):58-70.

PMID: 39811626 PMC: 11726452. DOI: 10.1038/s44220-024-00354-7.

Distinctive Neural Substrates of low and high Risky Decision Making: Evidence from the Balloon Analog Risk Task.

Jin Z, Li S, Wang C, Chai X, Zhang J, Li L Brain Topogr. 2024; 38(1):18.

PMID: 39625684 DOI: 10.1007/s10548-024-01094-8.

A new framework for understanding stress and disease: the developmental model of stress as applied to multiple sclerosis.

Fauver M, Clark E, Schwartz C Front Integr Neurosci. 2024; 18:1365672.

PMID: 38957213 PMC: 11218666. DOI: 10.3389/fnint.2024.1365672.

Abnormalities of brain structure and function in cervical spondylosis: a multi-modal voxel-based meta-analysis.

Cheng L, Zhang J, Xi H, Li M, Hu S, Yuan W Front Neurosci. 2024; 18:1415411.

PMID: 38948928 PMC: 11211609. DOI: 10.3389/fnins.2024.1415411.

Sleep disturbances, altered brain microstructure and chronic headache in youth.

Vandergaag I, Nania C, Timmers I, Simons L, Lebel C, Rasic N Brain Imaging Behav. 2024; 18(4):875-883.

PMID: 38558207 DOI: 10.1007/s11682-024-00876-9.

References

Teicher M, Samson J, Anderson C, Ohashi K . The effects of childhood maltreatment on brain structure, function and connectivity. Nat Rev Neurosci. 2016; 17(10):652-66. DOI: 10.1038/nrn.2016.111. View

Docherty M, Boxer P, Huesmann L, OBrien M, Bushman B . Assessing Callous-Unemotional Traits in Adolescents: Determining Cutoff Scores for the Inventory of Callous and Unemotional Traits. J Clin Psychol. 2016; 73(3):257-278. PMC: 7219563. DOI: 10.1002/jclp.22313. View

Tyborowska A, Volman I, Smeekens S, Toni I, Roelofs K . Testosterone during Puberty Shifts Emotional Control from Pulvinar to Anterior Prefrontal Cortex. J Neurosci. 2016; 36(23):6156-64. PMC: 6604884. DOI: 10.1523/JNEUROSCI.3874-15.2016. View

Smith S, Nichols T . Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2008; 44(1):83-98. DOI: 10.1016/j.neuroimage.2008.03.061. View

Smeekens S, Riksen-Walraven J, van Bakel H . Multiple determinants of externalizing behavior in 5-year-olds: a longitudinal model. J Abnorm Child Psychol. 2007; 35(3):347-61. PMC: 1915644. DOI: 10.1007/s10802-006-9095-y. View

Malter Cohen M, Tottenham N, Casey B . Translational developmental studies of stress on brain and behavior: implications for adolescent mental health and illness?. Neuroscience. 2013; 249:53-62. PMC: 3696429. DOI: 10.1016/j.neuroscience.2013.01.023. View

De Brito S, Viding E, Sebastian C, Kelly P, Mechelli A, Maris H . Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children. J Child Psychol Psychiatry. 2012; 54(1):105-12. DOI: 10.1111/j.1469-7610.2012.02597.x. View

Tottenham N, Sheridan M . A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci. 2010; 3:68. PMC: 2813726. DOI: 10.3389/neuro.09.068.2009. View

Li H, Li W, Wei D, Chen Q, Jackson T, Zhang Q . Examining brain structures associated with perceived stress in a large sample of young adults via voxel-based morphometry. Neuroimage. 2014; 92:1-7. DOI: 10.1016/j.neuroimage.2014.01.044. View

10.

McEwen B . Brain on stress: how the social environment gets under the skin. Proc Natl Acad Sci U S A. 2012; 109 Suppl 2:17180-5. PMC: 3477378. DOI: 10.1073/pnas.1121254109. View

11.

Nguyen T, McCracken J, Ducharme S, Botteron K, Mahabir M, Johnson W . Testosterone-related cortical maturation across childhood and adolescence. Cereb Cortex. 2012; 23(6):1424-32. PMC: 3643718. DOI: 10.1093/cercor/bhs125. View

12.

Ono M, Kikusui T, Sasaki N, Ichikawa M, Mori Y, Murakami-Murofushi K . Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male Balb/c mice. Neuroscience. 2008; 156(4):1103-10. DOI: 10.1016/j.neuroscience.2008.07.078. View

13.

Dziedzic N, Ho A, Adabi B, Foilb A, Romeo R . Shifts in hormonal stress reactivity during adolescence are not associated with changes in glucocorticoid receptor levels in the brain and pituitary of male rats. Dev Neurosci. 2014; 36(3-4):261-8. DOI: 10.1159/000362873. View

14.

Chen Y, Fu K, Feng C, Tang L, Zhang J, Huan Y . Different regional gray matter loss in recent onset PTSD and non PTSD after a single prolonged trauma exposure. PLoS One. 2012; 7(11):e48298. PMC: 3498281. DOI: 10.1371/journal.pone.0048298. View

15.

McCormick C, Mathews I, Thomas C, Waters P . Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn. 2009; 72(1):73-85. DOI: 10.1016/j.bandc.2009.06.003. View

16.

Sapolsky R, Krey L, McEwen B . The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev. 1986; 7(3):284-301. DOI: 10.1210/edrv-7-3-284. View

17.

Tamnes C, Ostby Y, Fjell A, Westlye L, Due-Tonnessen P, Walhovd K . Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex. 2009; 20(3):534-48. DOI: 10.1093/cercor/bhp118. View

18.

Sebastian C, De Brito S, McCrory E, Hyde Z, Lockwood P, Cecil C . Grey Matter Volumes in Children with Conduct Problems and Varying Levels of Callous-Unemotional Traits. J Abnorm Child Psychol. 2015; 44(4):639-49. PMC: 4830891. DOI: 10.1007/s10802-015-0073-0. View

19.

Lupien S, McEwen B, Gunnar M, Heim C . Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 2009; 10(6):434-45. DOI: 10.1038/nrn2639. View

20.

Carrion V, Wong S . Can traumatic stress alter the brain? Understanding the implications of early trauma on brain development and learning. J Adolesc Health. 2012; 51(2 Suppl):S23-8. DOI: 10.1016/j.jadohealth.2012.04.010. View