Pubertal onset as a critical transition for neural development and cognition

doi:10.1016/j.brainres.2016.04.012

Brain Research

Volume 1654, Part B, 1 January 2017, Pages 87-94

https://doi.org/10.1016/j.brainres.2016.04.012 Get rights and content

Highlights

•
Pruning occurs in the prefrontal cortex of adolescent humans and rats.
•
White matter increases throughout adolescence.
•
Evidence indicates that pubertal onset affects reorganization in the cortex.
•
Puberty may also impact the development of inhibitory control.
•
Documentation of pubertal status is valuable when studying adolescence.

Abstract

Adolescence, broadly defined as the period between childhood and adulthood, is characterized by a variety of neuroanatomical and behavioral changes. In human adolescents, the cerebral cortex, especially the prefrontal cortex, decreases in size while the cortical white matter increases. Puberty appears to be an important factor in both of these changes. However, the white matter continues to grow beyond what is thought to be adolescence, while the gray matter of the cortex stabilizes by young adulthood. The size changes that are the manifestation of cortical reorganization during human adolescence are also seen in cellular reorganization in the rat cortex. The prefrontal cortex loses neurons, dendrites and synapses while myelination in the white matter continues to increase. All of this reorganization is more marked in female rats, and there is evidence both from pubertal timing and from removal of the ovaries that puberty plays an important role in initiating these changes in females. The maturation of behavioral functions of the prefrontal cortex, such as inhibitory control, occurs in both humans and rats across adolescence. There is also evidence for puberty as a major factor in decreasing perseveration in rats, but few studies have been done using pubertal status as an experimental variable, and the role of the gonadal steroids in modulating behavior throughout life makes clear effects more difficult to document. In all, puberty appears to be so essential to the changes occurring during adolescence that it should be recorded when possible, especially given the sex difference in pubertal timing.

This article is part of a Special Issue entitled SI: Adolescent plasticity.

Introduction

Adolescence is the period between childhood and adulthood, characterized by neural maturation and changes in a variety of cognitive behaviors in addition to reproductive behavior. While it is obvious that libido and sexual behavior are set into motion by puberty, it is less apparent that pubertal onset is also involved in the maturation of the cerebral cortex and executive functions that occur during adolescence. It is difficult to establish the role of puberty in these changes in human adolescents where pubertal indices unfold over many years (Marshall and Tanner, 1969, Marshall and Tanner, 1970). In addition, specific information regarding pubertal status is often unavailable, especially for autopsy tissue where the cellular underpinnings of the loss of cortical volume can be examined. We will focus on cortical development and work from our laboratory in this review. We will present evidence from both human and animal models that puberty is an important event for many of the neural and behavioral changes that occur during adolescence.

Section snippets

Humans

Several MRI studies have indicated that the human cerebral cortex decreases in size during adolescence (Jernigan et al., 1991, Giedd et al., 1999, Sowell et al., 1999). While this appears to occur across many cortical areas, the prefrontal cortex (PFC) has the most reliably large decrease (Sowell et al., 2003, Gogtay et al., 2004), and this is especially interesting given that behaviors mediated by the PFC in particular undergo maturation during this time (Durston and Casey, 2006). There was a

Hormone receptors

One obvious question is which hormone receptors are present peripuberally in the cerebral cortex, particularly within the mPFC. This very relevant topic has not been directly explored in the existing literature. In the adult human temporal cortex, both males and females have moderate levels estrogen receptor (ER) α and ERβ (González et al., 2007). It is not known if these receptors are present in the PFC or if they are expressed during the pubertal transition. Like estrogen receptors, androgen

Adolescence

The adolescent period in humans is known to be associated with changes in performance on a variety of tasks, especially those that are PFC-dependent. Notably, cognitive control, defined as situationally appropriate behavioral responses in the face of conflicting ones, improves considerably between the juvenile period and adulthood (see Durston and Casey, 2006). Included within this definition is behavioral inhibition and cognitive flexibility, which coincide with a decrease in perseverative

Conclusions

There is considerable evidence that puberty is a central event in the reorganization of the cortex, especially the prefrontal cortex, during adolescence in both humans and rats. The evidence for the role of pubertal onset in the maturation of the functions of the cortex is less definitive, given the paucity of studies done where puberty was used as an experimental variable. Still, many types of behavior are influenced by gonadal steroids throughout life, suggesting that puberty could affect

Acknowledgments

The recent unpublished work was supported by NIH MH099625 to JMJ and NIH Training Grant T32 ES007326 currently supports JW. The authors have no conflicts of interest to report.

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View all citing articles on Scopus

View full text

ReviewPubertal onset as a critical transition for neural development and cognition

Highlights

Abstract

Introduction

Section snippets

Humans

Hormone receptors

Adolescence

Conclusions

Acknowledgments

Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats

Synapse

A comparison of adult and adolescent rat behavior in operant learning, extinction, and behavioral inhibition paradigms

Behav. Neurosci.

Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level

Cereb. Cortex

Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study

Arch. Gen. Psychiatry

The role of puberty in the developing adolescent brain

Hum. Brain Mapp.

Synaptogenesis in the prefrontal cortex of rhesus monkeys

Cereb. Cortex

Developmental changes in human cerebral functional organization for word generation

Cereb. Cortex

Beyond simple models of self-control to circuit-based accounts of adolescent behavior

Annu. Rev. Psychol.

Early metabolic programming of puberty onset: Impact of changes in postnatal feeding and rearing conditions on the timing of puberty and the development of the hypothalamic kisspeptin system

Endocrinology

Puberty in the corpus callosum

Neuroscience

Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers

Radiology

Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat

J. Comp. Neurol.

Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence

J. Comp. Neurol.

Development of cognitive control and executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition and task switching

Neuropsychologia

Changes in the number of synapses in the medial prefrontal cortex across adolescence

Society for Neuroscience Meeting, Chicago, Abstract

What have we learned about cognitive development from neuroimaging?

Neuropsychologia

Immunoreactivity for intracellular androgen receptors in identified subpopulations of neurons, astrocytes and oligodendrocytes in primate prefrontal cortex

J. Neurobiol.

A new approach to understanding the molecular mechanisms through which estrogens affect cognition

Biochim. Biophys. Acta

Brain development during childhood and adolescence: a longitudinal MRI study

Nat. Neurosci.

Synaptophysin and postsynaptic density protein 95 in the human prefrontal cortex from mid-gestation into early adulthood

Neuroscience

Dynamic mapping of human cortical development during childhood through early adulthood

Proc. Natl. Acad. Sci.

Distribution patterns of estrogen receptor alpha and beta in the human cortex and hippocampus during development and adulthood

J. Comp. Neurol.

Age and sex differences in reward behavior in adolescent and adult rats

Dev. Psychobiol.

The impact of sex, puberty, and hormones on white matter microstructure in adolescents

Cereb. Cortex

A longitudinal study: changes in cortical thickness and surface area during pubertal maturation

Plos One

Synaptic density in human frontal cortex- developmental changes and effects of aging

Brain Res.

The ontogeny of excitatory amino acid receptors in rat forebrain- I. N-methyl-d-aspartate and quisqualate receptors

Neuroscience

Maturation of human cerebrum observed in vivo during adolescence

Brain

Hormones and memory

Sexually dimorphic cognitive style in rats emerges after puberty

Brain Res. Bull.

Sex differences in the development of axon number in the splenium of the rat corpus callosum from postnatal day 15 through 60

Brain Res. Dev. Brain Res.

Increased functional connectivity with puberty in the mentalising network involved in social emotion processing

Horm. Behav.

Preputial separation as an external sign of pubertal development in the male rat

Biol. Reprod.

Delayed alternation in adolescent and adult male and female rats

Dev. Psychobiol.

Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats

Synapse

Gonadectomy before puberty increases the number of neurons and glia in the medial prefrontal cortex of female, but not male, rats

Review
Pubertal onset as a critical transition for neural development and cognition