Review
The impact of adolescent stress experiences on neurobiological development

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Abstract

Adolescence is considered a developmental period of heightened vulnerability to many psychological dysfunctions–primarily due to the high structural neuronal plasticity that accompanies the associated physical and cognitive gains, rendering an individual highly susceptible to environmental stressors during this time.

Recently, interest has been generated in the study of neuronal and behavioral adaptation to adverse experiences during adolescence. This review will provide an overview of the principal neurobehavioral changes that occur during adolescence and describe what happens when the maturation of these functions is altered by stressful environmental stimuli.

Introduction

The experience of adversities in early life is a predictor of a wide variety of pathological conditions, from psychiatric disorders, such as anxiety, depression, substance use disorders, schizophrenia, and autism spectrum disorders, to pathologies that are influenced by stress, such as cardiovascular disease, diabetes mellitus, and obesity [1], [2], [3], [4]. The World Health Organization (WHO) World Mental Health (WMH) Survey Initiative has reported that childhood adversities account for approximately 30% of all instances of first onset of mental disorders in 21 countries [5].

Notably, when disorders are associated with a history of childhood or adolescent trauma, they often present with severe symptomatology and resistance to conventional treatment [6], suggesting different etiological mechanisms. This profile highlights the importance of examining the neurobiological adaptations that lower an individual’s threshold to disease susceptibility. What renders the experience of a childhood/adolescent trauma a permanent modifier of individual health is that it acts on the plastic developing brain, which is prone to encoding environmental information into structural and functional modifications.

Throughout postnatal development, the brain undergoes dynamic changes in its epigenetic code, gene expression patterns, neural circuitry, and behavior [7]. These alterations facilitate the completion of stage-specific prerogatives: the formation of mother-attachment bonds in infancy, exploration of the environment, and social interactions with conspecifics during juvenile age.

The developmental framework of the postnatal brain is not genetically determined–rather, it interacts highly with the surrounding environment and is driven plastically by external inputs through gene-environment interplay to finely shape brain connections in their final form, allowing it to cope with similar environments later in life.

Neural and behavioral plasticity is transient and limited to sensitive periods during which various neural systems and behaviors are particularly receptive to several types of experience [8], [9]. Thus, a stressful experience during postnatal development–an abrupt variation in the environmental context in which the organism is gradually adapting–causes developmental imbalances that are strictly dependent on the timing in which the stress occurs. In this review, we will focus on adolescence, a developmental period of intense neuroplasticity and thus of heightened vulnerability to many psychological dysfunctions. We will introduce the most relevant behavioral components and the critical neural systems that develop during adolescence and are thus particularly sensitive to environmental stressors.

We will give an overview of the long-term effects that environmental stressors have during this time and can predispose one to or protect one from mental illness through their interaction with individual genetic factors.

Section snippets

Adolescence and the maturation of complex behaviors

Adolescence is a unique time for brain development, when, under environmental guidance, important neurobehavioral changes occur that appear to have a significant effect on motivation and emotions. During adolescence (from age 10–18 in humans), several dramatic neurophysiological and hormonal alterations take place, becoming substrates for behavioral changes, such as increases in sociability, impulsivity, and reward sensitivity [10], [11], [12]. In this developmental stage, the individual

Modeling the exposure to adverse stressful environments in adolescent rodents

Animal models provide an essential substrate for examining the neurobiological changes that are induced by early-life stressful experiences and tailoring preventive interventions. Reproducing adverse early-life events in rodents, such as losses, maltreatment, and abuse, has evident limits, due to the heterogeneity of experiences, differences in individual perceptions, and the strictly human nature of certain traumatic conditions. Modeling traumatic childhood or adolescence aims to understand

Effects of adolescent stress on behavioral components: emotionality, sociability, and reward sensitivity

Disruption of social environment and limitations in social play, a highly pleasurable, rewarding, and developmentally important activity for adolescent rodents [30], [31], alter many behavioral parameters, such as sociability, emotionality, and reward sensitivity, in adulthood. Moreover social experiences during adolescence induce persistent neurobiological changes that alter the sensitivity to the positive subjective and reinforcing properties of most, if not all, drugs of abuse [32].

In

Conclusions

Adolescence is a postnatal developmental period during which environmental factors have a profound impact on the maturation of an organism. Thus, stressful events during this time are likely to engender a risk for psychopathologies in adult life., This is due primarily to the extensive plasticity of the neurocircuits that regulate and control adult behaviors that are relevant to psychiatry, such as the corticolimbic system, reward system, and HPA axis.

As discussed in this review, postnatal

Acknowledgements.

We thank Clarissa Catale, Silvia Bussone and Fabiana Perrone for their help in writing the review.

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