Sleep EEG changes during adolescence: An index of a fundamental brain reorganization

Delta (1–4 Hz) EEG power in non-rapid eye movement (NREM) sleep declines massively during adolescence. This observation stimulated the hypothesis that during adolescence the human brain undergoes an extensive reorganization driven by synaptic elimination. The parallel declines in synaptic density, delta wave amplitude and cortical metabolic rate during adolescence further support this model. These late brain changes probably represent the final ontogenetic manifestation of nature’s strategy for constructing nervous systems: an initial overproduction of neural elements followed by elimination. Errors in adolescent brain reorganization may cause mental illness; this could explain the typical age of onset of schizophrenia. Longitudinal studies of sleep EEG are enhancing our knowledge of adolescent brain maturation. Our longitudinal study of sleep EEG changes in adolescence showed that delta power, which may reflect frontal cortex maturation, begins its decline between ages 11 and 12 years and falls by 65% by age 17 years. In contrast, NREM theta power begins its decline much earlier. Delta and theta EEG frequencies are important to sleep theory because they behave homeostatically. Surprisingly, these brain changes are unrelated to pubertal maturation but are strongly linked to age. In addition to these (and other) maturational EEG changes, sleep schedules in adolescence change in response to a complex interaction of circadian, social and other influences. Our data demonstrate that the daytime sleepiness that emerges in adolescence is related to the decline in NREM delta as well as to altered sleep schedules. These longitudinal sleep data provide guideposts for studying cognitive and behavioral correlates of adolescent brain reorganization.     

Development of the social brain during adolescence

Adolescence is usually defined as the period of psychological and social transition between childhood and adulthood. The beginning of adolescence, around the onset of puberty, is characterized by large hormonal and physical changes. The transition from childhood to adulthood is also characterized by psychological changes in terms of identity, self-consciousness, and cognitive flexibility. In the past decade, it has been demonstrated that various regions of the human brain undergo development during adolescence and beyond. Some of the brain regions that undergo particularly protracted development are involved in social cognitive function in adults. In the first section of this paper, I briefly describe evidence for a circumscribed network of brain regions involved in understanding other people. Next, I describe evidence that some of these brain regions undergo structural development during adolescence. Finally, I discuss recent studies that have investigated social cognitive development during adolescence.     

Development of the self-concept during adolescence

Adolescence is a period of life in which the sense of 'self' changes profoundly. Here, we review recent behavioural and neuroimaging studies on adolescent development of the self-concept. These studies have shown that adolescence is an important developmental period for the self and its supporting neural structures. Recent neuroimaging research has demonstrated that activity in brain regions associated with self-processing, including the medial prefrontal cortex, changes between early adolescence and adulthood. These studies indicate that neurocognitive development might contribute to behavioural phenomena characteristic of adolescence, such as heightened self-consciousness and susceptibility to peer influence. We attempt to integrate this recent neurocognitive research on adolescence with findings from developmental and social psychology.     

The development of gyrification in childhood and adolescence

Gyrification is the process by which the brain undergoes changes in surface morphology to create sulcal and gyral regions. The period of greatest development of brain gyrification is during the third trimester of pregnancy, a period of time in which the brain undergoes considerable growth. Little is known about changes in gyrification during childhood and adolescence, although considering the changes in gray matter volume and thickness during this time period, it is conceivable that alterations in the brain surface morphology could also occur during this period of development. The formation of gyri and sulci in the brain allows for compact wiring that promotes and enhances efficient neural processing. If cerebral function and form are linked through the organization of neural connectivity, then alterations in neural connectivity, i.e., synaptic pruning, may also alter the gyral and sulcal patterns of the brain. This paper reviews developmental theories of gyrification, computational techniques for measuring gyrification, and the potential interaction between gyrification and neuronal connectivity. We also present recent findings involving alterations in gyrification during childhood and adolescence.     

Do Cognitive Changes Accompany Developments in the Adolescent Brain?

ABSTRACT— The news that the brain continues to develop through much of adolescence risks becoming an explanation for anything and everything about teenagers and suggests the need for closer analysis. Central to such analysis is clarifying what develops at a psychological level during these years. An examination of contemporary research data on adolescent cognitive development identifies increased executive control as a major dimension of cognitive development during the second decade of life. Such development is consistent with changes occurring in the brain during this period.     

内外动机对青少年记忆的影响及其神经机制

动机是一切行为的核心, 动机可分为外在和内在动机。青少年时期既是记忆的关键期, 也是动机发展的特殊时期。然而, 目前关于内外动机影响青少年记忆的研究才刚刚起步, 尚不清楚外在和内在动机影响青少年记忆的规律和机制是否一致, 也不清楚二者如何交互影响记忆。本研究将结合认知范式和脑成像技术, 考察外在和内在动机如何分别影响以及交互影响青少年记忆。这将有助于更加全面、深刻理解内外动机影响青少年记忆的独特规律和机制, 为科学提升青少年动机和记忆效果提供研究证据。     

青少年抑郁及其自动情绪调节的研究概述

本文旨在梳理近年来国内外青少年抑郁及其自动情绪调节在相关研究领域的研究成果,以进一步促进青少年抑郁的自动情绪调节研究。首先,阐明了青少年脑发展与抑郁之间的关系,并概括了三种青少年抑郁模型。然后,澄清了自动情绪调节的内涵和经典范式,而且从时间和空间方面,总结了青少年抑郁的自动情绪调节的神经机制的相关文献。最后,未来要加强功能连接研究,采用经颅直流电刺激(t DCS)、重复经颅磁刺激(r TMS)技术开展干预研究。     

Enduring deficits in contextual and auditory fear conditioning after adolescent, not adult, social instability stress in male rats

Adolescence is a time of developmental changes and reorganization in the brain and stress systems, thus, adolescents may be more vulnerable than adults to the effects of chronic mild stressors. Most studies, however, have not directly compared stress experienced in adolescence to the same stress experience in adulthood. In the present study, adolescent (n=46) and adult (n=48) male rats underwent 16 days of social instability stress (daily 1h isolation and change of cage partners) or were non-stress controls. Rats were then tested on the strength of acquired contextual and cued fear conditioning, as well as extinction learning, beginning either the day after the stress procedure or 3 weeks later. No difference was found among the groups during the Training Phase of conditioning. Irrespective of the time between the social stress experience and fear conditioning, rats stressed in adolescence had decreased context and cue memory, and cue generalization compared to control rats, as measured by the percentage of time spent freezing in tests. Social instability stress in adulthood had no effect on any measure of fear conditioning. The results support the hypothesis that adolescence is a time of heightened vulnerability to stressors.     

Examining the link between adolescent brain development and risk taking from a social–developmental perspective

The adolescent age period is often characterized as a health paradox because it is a time of extensive increases in physical and mental capabilities, yet overall mortality/morbidity rates increase significantly from childhood to adolescence, often due to preventable causes such as risk taking. Asynchrony in developmental time courses between the affective/approach and cognitive control brain systems, as well as the ongoing maturation of neural connectivity are thought to lead to increased vulnerability for risk taking in adolescence. A critical analysis of the frequency of risk taking behaviors, as well as mortality and morbidity rates across the lifespan, however, challenges the hypothesis that the peak of risk taking occurs in middle adolescence when the asynchrony between the different developmental time courses of the affective/approach and cognitive control systems is the largest. In fact, the highest levels of risk taking behaviors, such as alcohol and drug use, often occur among emerging adults (e.g., university/college students), and highlight the role of the social context in predicting risk taking behavior. Moreover, risk taking is not always unregulated or impulsive. Future research should broaden the scope of risk taking to include risks that are relevant to older adults, such as risky financial investing, gambling, and marital infidelity. In addition, a lifespan perspective, with a focus on how associations between neural systems and behavior are moderated by context and trait-level characteristics, and which includes diverse samples (e.g., divorced individuals), will help to address some important limitations in the adolescent brain development and risk taking literature.     

The triadic systems model perspective and adolescent risk taking

In this special issue, Ernst (2014) outlines the triadic systems model, which focuses on the balanced interaction among three functional neural systems: the prefrontal cortex (regulation/control), striatum (motivation/approach), and amygdala (emotion/avoidance). Asynchrony in maturation timelines, coupled with less mature connectivity across brain regions, is thought to result in unique vulnerabilities for risk taking during the adolescent age period. Yet, the research evidence linking the triadic systems model to differences in risk taking across adolescence and adulthood is equivocal, and few studies have examined how neural development is associated with real-world behavior. In this commentary, we outline research on adolescent risk taking which highlights the importance of considering trait level and situational conditions when examining associations between neural systems and behavior, as well as the need to adopt a lifespan perspective.     

Examining the link between adolescent brain development and risk taking from a social–developmental perspective (reprinted)

The adolescent age period is often characterized as a health paradox because it is a time of extensive increases in physical and mental capabilities, yet overall mortality/morbidity rates increase significantly from childhood to adolescence, often due to preventable causes such as risk taking. Asynchrony in developmental time courses between the affective/approach and cognitive control brain systems, as well as the ongoing maturation of neural connectivity are thought to lead to increased vulnerability for risk taking in adolescence. A critical analysis of the frequency of risk taking behaviors, as well as mortality and morbidity rates across the lifespan, however, challenges the hypothesis that the peak of risk taking occurs in middle adolescence when the asynchrony between the different developmental time courses of the affective/approach and cognitive control systems is the largest. In fact, the highest levels of risk taking behaviors, such as alcohol and drug use, often occur among emerging adults (e.g., university/college students), and highlight the role of the social context in predicting risk taking behavior. Moreover, risk taking is not always unregulated or impulsive. Future research should broaden the scope of risk taking to include risks that are relevant to older adults, such as risky financial investing, gambling, and marital infidelity. In addition, a lifespan perspective, with a focus on how associations between neural systems and behavior are moderated by context and trait-level characteristics, and which includes diverse samples (e.g., divorced individuals), will help to address some important limitations in the adolescent brain development and risk taking literature.     

Synelfin Regulation during the Critical Period for Song Learning in Normal and Isolated Juvenile Zebra Finches

Male zebra finches (Taeniopygia guttata) learn to sing during a critical period in adolescence. We previously described a presynaptic protein, synelfin, whose mRNA is increased early in this critical period in a brain nucleus specifically implicated in song learning, lateral MAN (lMAN). In the current study, in situ hybridization was used to map this change in gene expression to the subregion of lMAN that projects to the robust nucleus of the archistriatum (RA), the principal motor output of the telencephalic circuit that controls song production. Using confocal immunofluorescence microscopy, we detected numerous puncta of synelfin immunoreactivity that apparently represent presynaptic terminals from lMAN in the RA of young males. Synelfin immunoreactivity in RA declined abruptly between 40 and 45 days of age, a time of major synaptic reorganization in RA. This change did not occur until about 10 days after the decline in synelfin mRNA in cell bodies within lMAN, indicating a relatively slow turnover of the protein in presynaptic terminals and suggesting that some of the functional changes that occur during the critical period may arise from regulatory decisions that were initiated a week or more earlier. Depriving birds of tutoring did not halt or delay the decline of synelfin mRNA in lMAN. This change in gene expression must not be a consequence of early song learning, but may reflect an innate or programmed step in song circuit development.     

The Adolescent Brain and the Emergence and Peak of Psychopathology

Adolescence is a period of heightened emotionality and increased risk for mental illness, affecting as many as one in five persons. This article reviews recent human imaging and animal studies that demarcate adolescent specific changes in brain and behavior that may help to explain this period of increased risk for psychopathology. We highlight adolescence as a sensitive period when: 1) the environment has particularly strong influences on brain and behavior and 2) normative changes in brain development can lead to an imbalance between rapidly changing limbic circuitry and relatively slower developing prefrontal circuitry. This imbalance can be exacerbated by both genetic and environmental influences leading to less capacity to regulate emotions and higher risk for psychopathology. We discuss these findings in the context of understanding who may be at greatest risk for psychopathology and when and how to best treat symptoms of emotional dysregulation.     

Changing brains, changing perspectives: the neurocognitive development of reciprocity

Adolescence is characterized by the emergence of advanced forms of social perspective taking and significant changes in social behavior. Yet little is known about how changes in social cognition are related to changes in brain function during adolescence. In this study, we investigated the neural correlates of social behavior during three phases of adolescence, carrying out functional magnetic resonance imaging of participants' brains while they were Player 2 in the Trust Game. We found that with age, adolescents were increasingly sensitive to the perspective of the other player, as indicated by their reciprocal behavior. These advanced forms of social perspective-taking behavior were associated with increased involvement of the left temporo-parietal junction and the right dorsolateral prefrontal cortex. In contrast, young adolescents showed more activity in the anterior medial prefrontal cortex, a region previously associated with self-oriented processing and mentalizing. These findings suggest that the asynchronous development of these neural systems may underlie the shift from thinking about self to thinking about the other.     

Sex differences in the adolescent brain

Adolescence is a time of increased divergence between males and females in physical characteristics, behavior, and risk for psychopathology. Here we will review data regarding sex differences in brain structure and function during this period of the lifespan. The most consistent sex difference in brain morphometry is the 9–12% larger brain size that has been reported in males. Individual brain regions that have most consistently been reported as different in males and females include the basal ganglia, hippocampus, and amygdala. Diffusion tensor imaging and magnetization transfer imaging studies have also shown sex differences in white matter development during adolescence. Functional imaging studies have shown different patterns of activation without differences in performance, suggesting male and female brains may use slightly different strategies for achieving similar cognitive abilities. Longitudinal studies have shown sex differences in the trajectory of brain development, with females reaching peak values of brain volumes earlier than males. Although compelling, these sex differences are present as group averages and should not be taken as indicative of relative capacities of males or females.     

The adolescent brain

Adolescence is a developmental period characterized by suboptimal decisions and actions that give rise to an increased incidence of unintentional injuries and violence, alcohol and drug abuse, unintended pregnancy and sexually transmitted diseases. Traditional neurobiological and cognitive explanations for adolescent behavior have failed to account for the nonlinear changes in behavior observed during adolescence, relative to childhood and adulthood. This review provides a biologically plausible conceptualization of the neural mechanisms underlying these nonlinear changes in behavior, as a heightened responsiveness to incentives while impulse control is still relatively immature during this period. Recent human imaging and animal studies provide a biological basis for this view, suggesting differential development of limbic reward systems relative to top-down control systems during adolescence relative to childhood and adulthood. This developmental pattern may be exacerbated in those adolescents with a predisposition toward risk-taking, increasing the risk for poor outcomes.     

Motor excitability is reduced prior to voluntary movements in children and adolescents with Tourette syndrome

Tourette syndrome (TS) is a neuro‐developmental disorder characterized by the occurrence of motor and vocal tics: involuntary, repetitive, stereotyped behaviours that occur with a limited duration, often typically many times in a single day. Previous studies suggest that children and adolescents with TS may undergo compensatory, neuroplastic changes in brain structure and function that help them gain control over their tics. In the current study we used single‐pulse and dual‐site paired‐pulse transcranial magnetic stimulation (TMS), in conjunction with a manual choice reaction time task that induces high levels of inter‐manual conflict, to investigate this conjecture in a group of children and adolescents with TS, but without co‐morbid Attention Deficit Hyperactivity Disorder (ADHD). We found that performance on the behavioural response‐conflict task did not differ between the adolescents with TS and a group of age‐matched typically developing individuals. By contrast, our study demonstrated that cortical excitability, as measured by TMS‐induced motor‐evoked potentials (MEPs), was significantly reduced in the TS group in the period immediately preceding a finger movement. This effect is interpreted as consistent with previous suggestions that the cortical hyper‐excitability that may give rise to tics in TS is actively suppressed by cognitive control mechanisms. Finally, we found no reliable evidence for altered patterns of functional inter‐hemispheric connectivity in TS. These results provide evidence for compensatory brain reorganization that may underlie the increased self‐regulation mechanisms that have been hypothesized to bring about the control of tics during adolescence.     

Development of eye-movement control

Cognitive control of behavior continues to improve through adolescence in parallel with important brain maturational processes including synaptic pruning and myelination, which allow for efficient neuronal computations and the functional integration of widely distributed circuitries supporting top-down control of behavior. This is also a time when psychiatric disorders, such as schizophrenia and mood disorders, emerge reflecting a particularly vulnerability to impairments in development during adolescence. Oculomotor studies provide a unique neuroscientific approach to make precise associations between cognitive control and brain circuitry during development that can inform us of impaired systems in psychopathology. In this review, we first describe the development of pursuit, fixation, and visually-guided saccadic eye movements, which collectively indicate early maturation of basic sensorimotor processes supporting reflexive, exogenously-driven eye movements. We then describe the literature on the development of the cognitive control of eye movements as reflected in the ability to inhibit a prepotent eye movement in the antisaccade task, as well as making an eye movement guided by on-line spatial information in working memory in the oculomotor delayed response task. Results indicate that the ability to make eye movements in a voluntary fashion driven by endogenous plans shows a protracted development into adolescence. Characterizing the transition through adolescence to adult-level cognitive control of behavior can inform models aimed at understanding the neurodevelopmental basis of psychiatric disorders.     

Adolescent Neurodevelopment and Psychopathology

Adolescence is a high-risk period for the onset of psychopathology. The occurrence of depression increases markedly in the years following the onset of puberty, and most individuals who are eventually diagnosed with a psychotic disorder show a marked rise in adjustment problems during adolescence. It is well established that puberty involves increases in the secretion of gonadal hormones. More recently, research has shown that stress hormones show a similar normative rise following puberty. Accumulating findings indicate that the postpubescent period is also characterized by significant neurodevelopment; there are changes in brain structure and function that are partially a consequence of hormonal factors. Researchers are now challenged to elucidate the neural mechanisms relating postpubertal neurodevelopment with the elevations in risk for psychopathology that characterize adolescence. One plausible mechanism is the effect of hormones on gene expression. The normal neuromaturational processes observed in adolescence partially reflect the effect of gonadal hormones on the expression of genes that control brain development. Hormone surges following puberty may also trigger the expression of genes that code for brain abnormalities that give rise to mental disorders.     

Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models

Developmental differences in hypothalamic–pituitary–adrenal (HPA) axis responsiveness to stressors and ongoing development of glucocorticoid-sensitive brain regions in adolescence suggest that similar to the neonatal period of ontogeny, adolescence may also be a sensitive period for programming effects of stressors on the central nervous system. Although research on this period of life is scarce compared to early life and adulthood, the available research indicates that effects of stress exposure during adolescence differ from, and may be longer-lasting than, effects of the same stress exposure in adulthood. Research progress in animal models in this field is reviewed including HPA function and the enduring effects of stress exposures in adolescence on sensitivity to drugs of abuse, learning and memory, and emotional behaviour in adulthood. The effects of adolescent stress depend on a number of factors, including the age, gender, the duration of stress exposure, the type of stressor, and the time between stress exposure and testing.