Elsevier

Brain Research

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

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

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

Highlights

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    Pruning occurs in the prefrontal cortex of adolescent humans and rats.

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    White matter increases throughout adolescence.

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    Evidence indicates that pubertal onset affects reorganization in the cortex.

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    Puberty may also impact the development of inhibitory control.

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    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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