Puberty and structural brain development in humans

doi:10.1016/j.yfrne.2016.12.003

Frontiers in Neuroendocrinology

Volume 44, January 2017, Pages 122-137

https://doi.org/10.1016/j.yfrne.2016.12.003 Get rights and content

Highlights

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Physical and hormonal markers of puberty have been linked with brain structure.
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Challenges are discussed, including capturing variability in hormone levels.
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More research is needed on individual differences in pubertal onset and progression.

Abstract

Adolescence is a transitional period of physical and behavioral development between childhood and adulthood. Puberty is a distinct period of sexual maturation that occurs during adolescence. Since the advent of magnetic resonance imaging (MRI), human studies have largely examined neurodevelopment in the context of age. A breadth of animal findings suggest that sex hormones continue to influence the brain beyond the prenatal period, with both organizational and activational effects occurring during puberty. Given the animal evidence, human MRI research has also set out to determine how puberty may influence otherwise known patterns of age-related neurodevelopment. Here we review structural-based MRI studies and show that pubertal maturation is a key variable to consider in elucidating sex- and individual- based differences in patterns of human brain development. We also highlight the continuing challenges faced, as well as future considerations, for this vital avenue of research.

Introduction

Puberty is an important period of development that occurs during adolescence. However, only recently has the notion been accepted that hormonal changes during puberty may continue to remodel and facilitate sexual differentiation of the brain. As outlined in a recent review (Juraska et al., 2013), sexual differentiation in mammals was originally thought to occur during a relative finite period of prenatal and early postnatal development, with sex-specific increases in testosterone leading to masculinization along with defeminization of the male brain. In recent years, however, animal studies on the impact of pubertal hormones have revealed that the brain continues to be remodeled and is even further sexually differentiated by sex steroids during pubertal development (see Juraska et al. (2013) for extensive review of the animal literature). Similarly, the field of neuroimaging has also begun to explore the role of puberty in human brain development. Here, we review the most up to date findings regarding pubertal maturation and typical brain development using magnetic resonance imaging (MRI). While it is important to note there are a number of physical growth and endocrine disorders that lead to early onset or delayed patterns of pubertal maturation (e.g. precocious puberty, Turner’s Syndrome, Klinefelter Syndrome, etc.) (Bramswig and Dubbers, 2009), these conditions are not reported on below as the current review aims to highlight the role puberty may have on brain maturation, above and beyond age, in typically developing adolescents.

Section snippets

Puberty

Puberty is a complex set of neuroendocrine processes that occur between childhood and adulthood to produce internal and external physical changes to primary and secondary sexual characteristics allowing for sexual reproduction. Puberty is initiated by reactivation of the hypothalamic-pituitary-gonadal (HPG) axis. During prenatal and early postnatal development, the HPG axis is responsible for sexual differentiation and organization of the central nervous system through its production of high

Common measurements of brain development using MRI

Advances in magnetic resonance imaging (MRI) have allowed for further understanding of how the brain continues to rapidly develop across adolescence. Using the same piece of equipment, various MRI sequences can collect images that allow for estimates of brain size, shape, and structural connectivity between distal regions. That is, structural MRI (T1-weighted imaging) can be used to quantify size and shape of gray and white matter areas. More specific to white matter, diffusion-weighted MRI,

Associations between pubertal development and brain volume

A number of cross-sectional studies have examined cortical and subcortical brain volumes based on grouping a narrowly defined age-range of individuals based on physical maturation scores, or correlating various puberty markers (including hormone levels and physical maturation scores) with brain volumes, while statistically controlling for age. A summary of these studies, including the age range and sample size of each study, can be found in Table 1. Below, we highlight some of the key findings

Summary and future directions

Review of the current literature on puberty and structural MRI highlights that both physical and hormonal changes during puberty are closely linked with changes in gray and white matter development. The noted inconsistencies among the correlational studies are likely multifactorial, including differences in age range, imaging methodology and analyses, as well as the limited ability to statistically disentangle the highly collinear factors of age and pubertal development. While still

Conclusions

The existing studies suggest that physical and hormonal changes during puberty are linked with unique patterns of structural brain maturation in humans. Furthermore, pubertal related changes seem to have differing effects on cortical versus subcortical limbic regions. The emerging evidence also suggests that future studies can help us to improve our understanding by designing studies aimed at better capturing hormone variance and individual differences in timing and progression of both physical

Acknowledgements

This research publication was supported in part by the National Institute of Mental Health and Eunice Kennedy Shriver National Institute of Child Health and Human Development of the National Institutes of Health under award number R01MH087563 (Sowell), K01MH1087610 (Herting), and F32HD078084 (Herting). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Review articlePuberty and structural brain development in humans

Highlights

Abstract

Introduction

Section snippets

Puberty

Common measurements of brain development using MRI

Associations between pubertal development and brain volume

Summary and future directions

Conclusions

Acknowledgements

Contraception

Neurotherapeutics

Brain Res.

J. Pediatr.

J. Pediatr.

Neuroscience

Steroids

Clin. Chim. Acta

J. Adolesc. Health

Neuroscience

Brain Cogn.

Brain Res.

J. Adolesc. Health

Psychoneuroendocrinology

J. Chem. Neuroanat.

NeuroImage

Horm. Behav.

Brain Res. Dev. Brain Res.

Psychoneuroendocrinology

Develop. Cognit. Neurosci.

Dev. Cogn. Neurosci.

J. Adolesc. Health

Neuroimage

Neuroimage

Brain Res. Mol. Brain Res.

J. Pediatr.

Horm. Behav.

Prog. Brain Res.

Horm. Behav.

Dev. Cogn. Neurosci.

Neuroimage

Psychoneuroendocrinology

Psychoneuroendocrinology

Psychoneuroendocrinology

J. Adolesc. Health Care

Dev. Cogn. Neurosci.

The optimal timing of blood collection during the menstrual cycle for the assessment of endogenous sex hormones: can interindividual differences in levels over the whole cycle be assessed on a single day?

Cancer Epidemiol. Biomarkers Prev.

Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions

Nat. Neurosci.

Laboratory testing of gonadal steroids in children

Pediatr. Endocrinol. Rev.

Sex-hormone-binding globulin

Clin. Endocrinol. (Oxf.)

Pubertal changes in hormone levels and depression in girls

Psychol. Med.

Puberty and depression: the roles of age, pubertal status and pubertal timing

Psychol. Med.

Diurnal rhythm of testosterone secretion before and throughout puberty in healthy girls: correlation with 17beta-estradiol and dehydroepiandrosterone sulfate

J. Clin. Endocrinol. Metab.

Changes of diurnal rhythm and levels of total and free testosterone secretion from pre to late puberty in boys: testis size of 3 ml is a transition stage to puberty

Eur. J. Endocrinol.

Serum steroids and pituitary hormones in female puberty: a partly longitudinal study

Clin. Endocrinol.

Hormonal pattern of adolescent menstrual cycles

J. Clin. Endocrinol. Metabol.

White matter development in adolescence: a DTI study

Cereb. Cortex

The importance of puberty for adolescent development: conceptualization and measurement

The role of puberty in the developing adolescent brain

Hum. Brain Mapp.

Self-assessment of pubertal stage in overweight children

Pediatrics

Review article
Puberty and structural brain development in humans