Developmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes

doi:10.1016/j.neubiorev.2011.04.013

Neuroscience & Biobehavioral Reviews

Volume 35, Issue 8, August 2011, Pages 1687-1703

https://doi.org/10.1016/j.neubiorev.2011.04.013 Get rights and content

Abstract

Adolescence is a transitional period between childhood and adulthood that encompasses vast changes within brain systems that parallel some, but not all, behavioral changes. Elevations in emotional reactivity and reward processing follow an inverted U shape in terms of onset and remission, with the peak occurring during adolescence. However, cognitive processing follows a more linear course of development. This review will focus on changes within key structures and will highlight the relationships between brain changes and behavior, with evidence spanning from functional magnetic resonance imaging (fMRI) in humans to molecular studies of receptor and signaling factors in animals. Adolescent changes in neuronal substrates will be used to understand how typical and atypical behaviors arise during adolescence. We draw upon clinical and preclinical studies to provide a neural framework for defining adolescence and its role in the transition to adulthood.

Highlights

► We review adolescence as a heterogeneous developmental stage. ► Neuroanatomical changes are juxtaposed with environmental influences and demands. ► Developmental trajectories interact with sex-dependent changes. ► We discuss the evolution of understanding with increasingly sensitive research tools.

Introduction

Adolescence is a special period in mammalian brain development. Understanding adolescence has been described in a number of reviews at the behavioral level (McCutcheon and Marinelli, 2009, Spear, 2000, Steinberg, 2010a, Steinberg, 2010b, Laviola et al., 1999, Laviola et al., 2003) and the systems level (Ernst and Fudge, 2009), but only discussed to a limited degree at the level of neuronal changes (Andersen, 2003, McCutcheon and Marinelli, 2009, O’Donnell, 2010, Spear, 2000). We will review the neuroanatomy, functional connectivity, genetics, and signaling changes that occur during adolescence. Subsequently, a framework within a neural systems approach will synthesize how adolescent changes in these markers influence behavior.

Section snippets

Defining adolescence

Adolescence can be defined as the period between 10 and 19 years of age in humans (WHO, 2010s), between 2 and 4 years in primates (Schwandt et al., 2007), and between 35 and 60 days of age in rodents (Andersen et al., 2000, McCutcheon and Marinelli, 2009). Spear (2000) begins her discussion of this period with typical adolescence defined as a behavioral transitional period. Such behavioral transitions are consistently observed across diverse mammalian species by an increased sensitivity to

The making of a trajectory: neuroanatomical changes

At the neuronal level, the process of adolescent brain development is one of synaptic refinement. Neurons are initially laid down in an inside-out pattern of innervation in the cortex (Rakic et al., 1986). Neurons that were first born innervate the deeper layers of the cortex, while innervation of the more superficial layers of the cortex occurs later in development. Neuronal targeting is guided by both glia cells (Rakic et al., 1986, Vernadakis, 1975) and chemical gradients that are determined

Specific innervation of neurotransmitter systems

In this section, we discuss how specific neurotransmitter systems innervate a given brain region. Innervation begins prenatally, but actively continues into the adolescent period and adulthood. However, most studies bypass characterizing adolescence and assume that innervation proceeds in a linear fashion. Human post-mortem studies of connectivity are nearly impossible to conduct, as brain tissue resource centers typically dissect brain tissues into smaller areas that prevent tract tracing. The

Functional development of circuits

During adolescence, dramatic shifts in behavior are tied to age-related changes within the brain. Extensive reviews of adolescent behaviors are found elsewhere (Spear, 2000), but we present a brief overview of how specific changes in functional processing during adolescence may explain some of these behaviors. Within the orchestration of building a brain, each region has its own developmental timecourse of maturation (Tau and Peterson, 2010). Generally, cortical areas mature later than

Experience shapes brain development

While genes provide the blueprint to construct the brain, experience sculpts that brain to match the needs of the environment. The final fate of a given synapse is based on functional validation. The adolescent brain is not only uniquely susceptible to environmental influences, but adolescence is also a period when early experiences manifest (Andersen, 2003, Andersen and Teicher, 2008). Complex neural networks form during adolescence, and these in turn are sculpted by both spontaneous and

Summary

The nature and extent of adolescent changes within brain neuroanatomy is constantly changing as our tools of analysis become more fine-grained. Diversity can only be fully appreciated when regions are studied within functional divisions (e.g., Gogtay et al., 2006), with complete timecourse of characterization, and when early experiences (Andersen and Teicher, 2008) and other factors (e.g., sex, Tanner stage) are taken into consideration. Incomplete timecourses in earlier studies have led to

Acknowledgement

Funded by NIH.

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ReviewDevelopmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes

Abstract

Highlights

Introduction

Section snippets

Defining adolescence

The making of a trajectory: neuroanatomical changes

Specific innervation of neurotransmitter systems

Functional development of circuits

Experience shapes brain development

Summary

Acknowledgement

Behav. Brain Res.

Neurosci. Biobehav. Rev.

Trends Pharmacol. Sci.

Trends Neurosci.

Neurosci. Biobehav. Rev.

Psychoneuroendocrinology

Neuroscience

Neuroimage

Eur. J. Pharmacol.

J. Magn. Reson. B

Neuroimage

Neuroimage

Neurosci. Biobehav. Rev.

Brain Res.

Neuron

Neurosci. Biobehav. Rev.

J. Am. Acad. Child Adolesc. Psychiatry

J. Affect. Disord.

Prev. Med.

Brain Res. Dev. Brain Res.

Neuroscience

Pharmacol. Biochem. Behav.

Neurosci. Biobehav. Rev.

Neuropsychologia

Neurosci. Lett.

J. Psychiatr. Res.

J. Am. Acad. Child Adolesc. Psychiatry

Biol. Psychiatry

Brain Res. Dev. Brain Res.

Neurosci. Biobehav. Rev.

Encephale

Neuroimage

Neuropsychologia

Biol. Psychol.

Pharmacol. Biochem. Behav.

Brain Res. Dev. Brain Res.

The enduring effects of abuse and related adverse experiences in childhood: a convergence of evidence from neurobiology and epidemiology

Eur. Arch. Psychiatry Clin. Neurosci.

Adverse childhood experiences, alcoholic parents, and later risk of alcoholism and depression

Psychiatr. Serv.

Maturational increases in c-fos expression in the ascending dopamine systems

Synapse

Sex differences in dopamine receptor overproduction and elimination

Neuroreport

Delayed effects of early stress on hippocampal development

Neuropsychopharmacology

Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats [In Process Citation]

Synapse

Inhibition of serotonin but not norepinephrine transport during development produces delayed, persistent perturbations of emotional behaviors in mice

J. Neurosci.

Emerging adulthood. A theory of development from the late teens through the twenties

Am. Psychol.

Toward a new understanding of attention-deficit hyperactivity disorder pathophysiology: an important role for prefrontal cortex dysfunction

CNS Drugs

White matter development in adolescence: a DTI study

Cereb. Cortex

Attention-deficit/hyperactivity disorder, self-regulation, and time: toward a more comprehensive theory

J. Dev. Behav. Pediatr.

Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making

J. Neurosci.

Common and distinct amygdala-function perturbations in depressed vs anxious adolescents

Arch. Gen. Psychiatry

Excitatory actions of gaba during development: the nature of the nurture

Nat. Rev. Neurosci.

Review
Developmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes