Puberty is an endocrinological event leading to sexual maturation.
In the process of achieving reproductive maturity, this surge in hormones plays a central role within a larger set of biological changes, which include rapid physical growth; sexually dimorphic alterations in facial structure, voice, and body characteristics; metabolic changes; the activation of new drives and motivations; changes in sleep and circadian regulation; and a wide array of social, behavioral, and emotional changes.
The start of puberty is characterized by the reactivation of the hypothalamic-pituitary-gonadal HPG axis. The first step is when the hypothalamus begins to release large amounts of gonadotropin-releasing hormone GnRH in a pulsatile manner during sleep Delemarre-van de Waal, The HPG axis is active during prenatal and early postnatal life and then becomes quiescent throughout childhood. Puberty actually represents a reactivation. The first outward signs of puberty are breast development in girls and genital development in boys.
The development of these secondary sexual characteristics occurs, on average, at age 10 in girls and age In addition to the gonadal hormones testosterone and estradiol, the adrenal androgen dehydroepiandrosterone DHEA also plays a role in the development of secondary sexual characteristics, including pubic hair girls and boys and facial hair boys; Delemarre-van de Waal, Changes in levels of growth hormone also contribute to pubertal growth and metabolic changes.
In addition, other neuroendocrine systems also appear to contribute to neurobehavioral changes during puberty. For example, oxytocin and vasopressin, involved in social bonding, appear to undergo changes in adolescence in some species. However, there is a dearth of data on humans that directly addresses these influences, so most of this review will focus on gonadal hormones.
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The development of reproductive capabilities involves not only changes in the body, but also changes in neural systems. The brain is a major target for sex-steroid hormones. Sex steroids act on the brain in two different ways: first, through organizational effects that permanently change the structure of the brain e. Until recently, it was believed that organizational effects of sex hormones took place only during prenatal and early postnatal life, and that puberty reflected only activational effects of sex hormones.
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However, recent animal work has shown clear evidence of further organizational effects during puberty, such as the addition of new neurons to parts of the hypothalamus and amygdala Ahmed et al. However, human studies have a limited capacity for disentangling the direct effects of hormones from indirect effects e. Accordingly, we will focus on activational effects of pubertal hormones, reviewing briefly the evidence for how specific hormones appear to influence behavior. Increased levels of testosterone during adolescence have been associated with increased approach-related behaviors, such as proactive aggression van Bokhoven et al.
With respect to brain activity, increased levels of testosterone in boys predict enhanced activation in the ventral striatum after high-risk gambles Op de Macks et al. However, there is also evidence that social rewards are particularly important during this period of development, given that pubertal testosterone is a strong predictor of status-relevant motivation and behavior.
These findings demonstrate that the social environment not only mediates the effects of testosterone on behavior but also influences actual levels of testosterone itself. For example, relatively high levels of testosterone, together with relatively low levels of cortisol, have been implicated in delinquent behavior in adolescent boys Popma et al.
The role of estradiol in motivated behavior in humans is less well studied than that of testosterone. The effects varied across the menstrual cycle: The association between estradiol and risk-taking was strongest during the mid-luteal phase, when estradiol levels are relatively high. Moreover, this effect was not seen until puberty, which indicates that it is dependent on the surge of hormones at puberty Quinlan et al.
Taken together, these data suggest that increased pubertal estradiol in females is related to lessened behavioral inhibition and increased risk taking. Moreover, with respect to the relation between brain activity and risk-taking, it was found that higher estradiol levels in girls predict stronger activity within the ventral striatum after high-risk gambles, although this effect of estradiol was somewhat weaker than that of testosterone in boys Op de Macks et al. This emphasis on social and affective influences is not intended to imply that these are the only neurobehavioral effects of pubertal hormones.
Clearly, some aspects of cognitive and social-cognitive function are impacted by pubertal hormones. This is quite interesting given that the anterior temporal lobe has been implicated in the processing of social emotions such as guilt and embarrassment Zahn et al. The model suggests that interactions between social-affective processing systems in the brain and cognitive-control systems can lead to healthy adaptation to the complex and rapidly changing social contexts of adolescence. However, these interactions can also lead to negative trajectories, such as substance abuse or depression.
Such negative trajectories may begin as small changes but, over time, can lead to patterns of behavior that have cascading effects: brain-behavior interactions with spiraling impact across adolescence. As a more in-depth illustration of how a small pubertal change in one neurobehavioral system can spiral into large-scale complex behavioral consequences, let us consider the powerful example of sleep and circadian changes during adolescent development.
In humans, there is evidence for a similar circadian shift in sleep preferences at puberty. The direct effect of these pubertal changes appears to be relatively subtle—for example, a typical midpubertal year-old may experience slight biological tendencies to prefer staying up later and to sleep in later on weekends.
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Moreover, for most of human history until the advent of electric lights , this slight tendency to prefer staying up later at night was unlikely to result in large, sustained effects on behavior because the prevailing darkness at night presented adolescents with limited opportunities to activate their hypothalamus with the type of light signals that create large-scale biological shifts in the circadian clock. However, in contemporary society, not only do youths have access to bright lights at any hour of the night, but it also appears that blue spectrum light from TV, computer, and personal-device screens may have particularly strong effects on the human circadian system.
Even more importantly, several other social and motivational factors increase the likelihood that many adolescents will use these arousing light-signaling devices later into the night Carskadon, Together, this combination of social and behavioral factors has contributed to a situation in the United States where the average school-night bedtime among high school seniors is after p. The resulting chronic sleep deprivation and catch-up sleep on weekends resulting in very late schedules further amplifies the spiral of negative effects.
Insufficient sleep has a cascade of negative effects on other aspects of emotion, behavior, cognition, and learning, which can, in turn, further interfere with the regulation of sleep and arousal Carskadon, The main point here is to illustrate how a relatively small pubertal change in particular neural systems—in this case, an increased circadian sensitivity to the environment light and social cues —can become amplified by multiple social factors across adolescence.
Thus, while the direct effects of the initial increase in pubertal hormones may appear relatively small, the longer-term effects on brain-behavior interactions can become large-scale effects over time.
This framework helps us understand why specific details about hormonal effects on neurobehavioral tendencies represent important scientific questions. If we extend this example to consider the impact of a small pubertal increase in the motivational salience of social status, we can imagine a similarly complex cascade of changes as with sleep patterns interacting with complex contemporary social contexts. Most importantly, it highlights the power of social and cultural influences e.
Clearly, a great deal more research is needed to empirically test features of this model—and to advance understanding of the specific hormonal mechanisms and specific neural systems that underlie these changes. Our most important conclusion is that more studies of adolescent brain development need to focus on puberty-specific and hormone-specific developmental processes. In addition, it requires further development and refinement of heuristic models and testing of key features of these models to advance our understanding of how specific hormones impact specific neural systems to influence specific behavioral tendencies.
Another important consideration entails recognizing that the biological signals created by a given hormone can sometimes have little to do with the level of the hormone in the blood or saliva, as opposed to the timing or pattern of hormone secretion. For example, it is well established that the fundamental trigger for the onset of puberty is the pulse frequency of gonadotropin-releasing hormone rather than the level of the hormone. Other priorities for future research include considering and investigating a broad range of hormones that change during puberty.
These include not only changes in estradiol, testosterone, and the adrenal androgens DHEA and DHEA sulphate but also changes in other neuroendocrine systems that appear to undergo developmental changes at puberty, such as growth-hormone regulation and hypothalamic-pituitary-adrenal-axis regulation. One particularly interesting line of investigation focuses on the oxytocin-vasopressin system that has been shown to be central to social-bonding motivation and behaviors and to influence social cognitive processes such as trust which it does differently in in-group and out-group contexts.
Given the dynamic social changes in adolescence—establishment of close friendships, intense motivations, and emotions associated with early sexual and romantic relationships, as well as changes in family relationships—it would be surprising if pubertal changes in these oxytocin and vasopressin systems were not intertwined with some of these developmental changes.
To conclude, our review demonstrates that pubertal hormones contribute to brain-behavior interactions. At least in some cases, these effects appear to be manifested as action tendencies, or behavioral tendencies, which can appear in some ways to have relatively subtle effects. Yet even small changes in behavioral tendencies e. There is growing evidence that these hormone-driven tendencies can impact long-term developmental trajectories in both positive and negative ways. Achieving a better understanding of these important developmental processes represents an exciting and pioneering area for transdisciplinary research.
Carskadon, M. See References. A comprehensive overview of what is known about sleep during pubertal transition and adolescent development. Josephs, R. A review that discusses socially and environmentally modulated effects on pubertal testosterone. Shirtcliff, E.
A thorough methodological paper that discusses various ways to quantify pubertal development in humans, each with its pros and cons. Declaration of Conflicting Interests The authors declared no conflicts of interest with respect to their authorship or the publication of this article.
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