Experience-dependent neurodevelopment of self-regulation in adolescence

Abstract

Adolescence is a period of rapid biobehavioral change, characterized in part by increased neural maturation and sensitivity to one's environment. In this review, we aim to demonstrate that self-regulation skills are tuned by adolescents' social, cultural, and socioeconomic contexts. We discuss adjacent literatures that demonstrate the importance of experience-dependent learning for adolescent development: environmental contextual influences and training paradigms that aim to improve regulation skills. We first highlight changes in prominent limbic and cortical regions-like the amygdala and medial prefrontal cortex-as well as structural and functional connectivity between these areas that are associated with adolescents' regulation skills. Next, we consider how puberty, the hallmark developmental milestone in adolescence, helps instantiate these biobehavioral adaptations. We then survey the existing literature demonstrating the ways in which cultural, socioeconomic, and interpersonal contexts drive behavioral and neural adaptation for self-regulation. Finally, we highlight promising results from regulation training paradigms that suggest training may be especially efficacious for adolescent samples. In our conclusion, we highlight some exciting frontiers in human self-regulation research as well as recommendations for improving the methodological implementation of developmental neuroimaging studies and training paradigms.

Keywords: Adolescence; Brain development; Puberty; Social context; Structural environment; Training.

Fig. 1

Conceptual diagram of adolescent neural adaptation and the influence of contextual factors on emotional neurodevelopment. Of special importance for affective learning and emotion regulation, corticolimbic connections are pruned over time while sensitivity to affective stimuli within specific prefrontal regions and the amygdala correspond with developmental stage. These changes promote adaptation as adolescents experience multiple contextual inputs from socioeconomic, interpersonal, and cultural influences. Double arrows reflect the capacity for forward- and backward-influence between contextual factors, brain adaptation and emotional skills. Figure created with inspiration from Ahmed et al. (2015) and Blakemore (2008). Brain graphic created with BioRender.com. In the neural adaptation portion, we highlight prominent regions discussed in relation to self-regulation development. From bottom right of neural adaptation brain figure (counterclockwise): amygdala, ventral striatum (VS), ventromedial prefrontal cortex (vmPFC), anterior cingulate cortex (ACC), dorsolateral prefrontal cortex (dlPFC), and temporal parietal junction (TPJ). Brief descriptions are provided below for each region. Amygdala: Multiple nuclei comprise this region, with connections to regions of vmPFC and dlPFC. The amygdala is associated with fear and threat responses as well as salience detection for affective stimuli. Ventral striatum (VS): A subcortical region interconnected with limbic regions (e.g., amygdala) and the prefrontal cortex. The ventral striatum is associated with evaluating reward and motivation for goal-oriented action (Silverman et al., 2015). The VS includes the nucleus accumbens, a portion adjacent to the septum that is implicated in reward processing through its involvement with action selection and integration of cognitive and affective information from distributed frontal and temporal regions (Floresco, 2015). Ventromedial prefrontal cortex (vmPFC): A subregion of the prefrontal cortex, vmPFC is a modulatory region, associated with extinguishing affective responses and engaging top-down systems for emotion responses and regulation (Buhle et al., 2014). Anterior cingulate cortex (ACC): A cortical region involved in executive function and emotion skills through extensive connections to regions of prefrontal cortex. The ACC is associated with goal maintenance and aspects of cognitive control (Gasquoine, 2013). Dorsolateral prefrontal cortex (dlPFC): Another subregion of the prefrontal cortex, the dlPFC is associated with aspects of attention and working memory. In relation to emotion regulation, it is thought to help maintain and update emotional information held in mind (Duncan and Owen, 2000). Temporal parietal junction (TPJ): Located along the border of temporal and parietal lobes, the temporal parietal junction serves as a nexus for multiple language, memory, and mentalizing. As such, the temporal parietal junction is a distinctly social brain region, providing social context to many behaviors, including emotionally laden social stimuli (Carter and Huettel, 2013).