Elsevier

Hormones and Behavior

Volume 64, Issue 2, July 2013, Pages 270-279
Hormones and Behavior

Review
Adolescent sleep patterns in humans and laboratory animals

https://doi.org/10.1016/j.yhbeh.2013.01.013Get rights and content

Abstract

This article is part of a Special Issue “Puberty and Adolescence”.

One of the defining characteristics of adolescence in humans is a large shift in the timing and structure of sleep. Some of these changes are easily observable at the behavioral level, such as a shift in sleep patterns from a relatively morning to a relatively evening chronotype. However, there are equally large changes in the underlying architecture of sleep, including a > 60% decrease in slow brain wave activity, which may reflect cortical pruning. In this review we examine the developmental forces driving adolescent sleep patterns using a cross-species comparison. We find that behavioral and physiological sleep parameters change during adolescence in non-human mammalian species, ranging from primates to rodents, in a manner that is often hormone-dependent. However, the overt appearance of these changes is species-specific, with polyphasic sleepers, such as rodents, showing a phase-advance in sleep timing and consolidation of daily sleep/wake rhythms. Using the classic two-process model of sleep regulation, we demonstrate via a series of simulations that many of the species-specific characteristics of adolescent sleep patterns can be explained by a universal decrease in the build-up and dissipation of sleep pressure. Moreover, and counterintuitively, we find that these changes do not necessitate a large decrease in overall sleep need, fitting the adolescent sleep literature. We compare these results to our previous review detailing evidence for adolescent changes in the regulation of sleep by the circadian timekeeping system (Hagenauer and Lee, 2012), and suggest that both processes may be responsible for adolescent sleep patterns.

Highlights

► Dramatic changes in sleep are a hallmark of adolescence in humans and animals. ► Both humans and animals show changes in sleep timing, architecture, and homeostasis. ► Many changes are driven by pubertal hormones and parallel cortical development. ► Universal changes in sleep homeostasis may underlie species-specific patterns.

Introduction

Sleep is arguably the primary activity of the developing brain (Dahl, 1998). During infancy, a time of rapid synaptogenesis and brain growth, individuals spend on average 13–16 h a day asleep. This average does not drop below 12 h until the age of four when cortical synaptic density plateaus. At ten years of age children still sleep for 10 h a day (Jenni and Carskadon, 2007). If sleep is critically tied to brain development, then characterizing sleep during adolescence should be of particular interest. Adolescence is not only a time of transition from a developing brain and body to adulthood, but also a complex and sensitive period that includes large hormonal fluctuations, permanent brain reorganization, and rapid growth (Sisk and Zehr, 2005, Spear, 2000). If the relationship between sleep and development is not merely correlational but essentially linked, then sleep deprivation during adolescence may permanently alter the developmental trajectory of the brain and behavior (Shaffery et al., 2006). Despite this possibility, many modern social and technological features compel teenagers in developed countries to be overwhelmingly and chronically sleep deprived (Andrade and Menna-Barreto, 2002, Giannotti and Cortesi, 2002, Gradisar et al., 2011, Thorleifsdottir et al., 2002, Yang et al., 2005).

For this reason, there has been growing scientific interest in the unique changes that characterize adolescent sleep patterns, with an eye on public health applications. As there have been several excellent recent reviews on this topic (Carskadon 2010; Colrain and Baker, 2011, Feinberg and Campbell, 2010), we will focus on a less discussed topic: similarities and differences in the manner that sleep patterns change during development across species. If we presume that many of the physiological events associated with puberty and adolescence are not events specific to humans but instead represent common changes necessary for achieving sexual maturity and independent life across mammalian species (Sisk and Zehr, 2005, Spear, 2000), many of the changes in sleep observed during adolescence in humans should be observable in common laboratory species. Indeed, using model species allows us to examine the hormonal and neural causes of adolescent sleep patterns in greater depth, as well as to characterize their developmental trajectory when isolated from social constraint and the influences of artificial lighting and modern technology.

Section snippets

Puberty & adolescence: humans vs. laboratory species

Before comparing adolescent sleep patterns across species, it is important to understand that the developmental progression of puberty and adolescence differs between humans and traditional laboratory species. Colloquially the terms “puberty” and “adolescence” are used interchangeably, but scientifically they refer to separate concepts (Sisk and Zehr, 2005). Traditionally, puberty is defined as the process leading to the attainment of sexual maturation (Spear, 2000), beginning with the

Sleep is regulated by homeostatic “sleep pressure” and a daily circadian rhythm

Traditionally, sleep patterns are thought to derive from three primary components: an internal (endogenous) daily circadian timekeeping system, a homeostatic drive for sleep (“sleep pressure”) that builds up over the course of being awake and decreases during sleep, and other external constraints (which are collectively referred to as “masking”). Both internal components are known to be sensitive to sex (gonadal) hormones, such as estrogen and testosterone (Hagenauer and Lee, 2012, Mong et al.,

Sleep pattern development in adolescent humans

For the sake of concise interspecies comparison, we will focus this review on the strongest insights provided from the human literature, as derived from extensive longitudinal naturalistic studies and smaller well-controlled laboratory studies. More detailed reviews can be found in Colrain and Baker (2011), Feinberg and Campbell (2010), and Carskadon (2011).

Sleep pattern development in laboratory animals

Sleep pattern development during adolescence in laboratory animals is less well-studied, but supports the assertion that other species show adolescent changes in sleep timing, architecture, and homeostasis, although these changes may not take the same form that they do in adolescent humans.

Discussion

Both humans and laboratory animals undergo large changes in sleep patterns during adolescence, including changes in sleep timing, sleep architecture, and sleep homeostasis. In our previous review, we discussed in detail how these changes might relate to hormonally-driven development of the circadian timekeeping system (Hagenauer and Lee, 2012). There are several pieces of evidence that suggest that the phasing of circadian output shifts during adolescence, paralleling the shift in sleep timing.

Acknowledgments

We would like to thank John Basler and Dr. Victoria Booth for their guidance and feedback regarding model construction. We would also like to thank Katherine Prater, Chelsea Fournier, Dr. Stephanie Crowley, and Dr. Jamie Perryman for their insightful feedback and editing. This research was supported by a grant from the National Science Foundation (TML, MHH — IBN-0952046) as well as an Endocrinology training grant from the National Institute of Health through the Department of Pediatrics at

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