Pubertal onset as a critical transition for neural development and cognition

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.

Keywords: Adolescence; Inhibitory control; Neuron number; Prefrontal cortex; Puberty.

Figure 1

The number of neurons in the rat mPFC at postnatal ages that encompass adolescence. (A) Females lost neurons between P35 and P45, and the average age of pubertal onset was P35. *p<.05. (B) Unlike the females, males only showed a nonsignificant trend (p<.08) for age. From Willing and Juraska, 2015.

Figure 2

The density of dendritic spines at postnatal ages on layer V pyramidal neurons in the mPFC a) on the basilar dendrites and b) on the apical dendrites. Spines were pruned between P35 and P90. There were no sex differences. c) A photograph of dendritic spines visualized with a Golgi Cox stain. *p<.05; #p<.08 From Koss et al. (2014).

Figure 3

The number of myelinated axons in the splenium of the corpus callosum quantified from electron micrographs. Females are clear bars and males stripped bars. **p<.005; ***p<.0005 From Kim and Juraska, 1997.

Figure 4

a) The number of neurons in the two subdivisions of the rat primary visual cortex (Oc1M and Oc1B) in adult rats. The control females had significantly (p<.05) fewer neurons in both divisions than control males and day 20 OVX females. Modified from Nunez et al., 2002. b) The number of neurons in the mPFC in adult rats. Gonadectomy (GDX) had occurred at P20. *p<.05 From Koss et al., 2015.

Figure 5

Path length to reach the novel platform location in the Morris water maze. Path length was significantly lower in post-pubertal males and females in comparison to prepubertal after the location of an escape platform was moved. a>b p<03 Modified from Willing et al., in press.