Review articleThe role of experience in adolescent cognitive development: Integration of executive, memory, and mesolimbic systems
Introduction
Adolescent neurodevelopment has garnered great attention because of the associated propensity towards increased risk taking behavior (e.g., unprotected sex, substance use) and the emergence of psychopathology (e.g., schizophrenia, mood disorders). Prevailing neurodevelopmental models agree that a relative predominance of reward processing over executive functions is core to increased exploration and sensation seeking in adolescence. These processes are thought to garner an adaptive stage of information seeking in service of obtaining experiences that support independence as adults (Shulman et al., 2016). The process of acquiring information to adapt to environmental demands is present throughout the lifespan. However, during adolescence there are unique elements of information seeking that define it as a unique period compared to earlier development and adulthood. The nature of the rewards that drive information seeking change across development (mother’s face in infancy, to professional satisfaction in adulthood, and social networking in adolescence). Further, the nature of information seeking is qualitatively different. Adolescents partake in sensation seeking behaviors (including exploration and novelty seeking) that incur a risk to survival to acquire new experiences, reflecting a unique quality to information seeking during this time of the lifespan. As proposed in prior neurodevelopmental models (Luna and Wright, 2016, Shulman et al., 2016), adolescents plan actions independent from the guidance of others that prioritize value of immediate rewards while suppressing information regarding negative consequences. By adulthood, the experiences that were accumulated in earlier development are integrated and organized in a manner to support reliable implementation. These prior models are based on a large developmental cognitive neuroscience literature that focuses on the maturation of prefrontal executive systems, dopamine systems associated with reward processing, and the nature of their interaction (Luna and Wright, 2016, Shulman et al., 2016). However, missing from these models are neurodevelopmental mechanisms that detail how adolescents are able to reliably use acquired experiences to support adult levels of cognition.
Here, we extend these prior models by integrating the function of hippocampal memory systems, which could support the ability for prior experiences to influence the specialization of prefrontal systems. Similar to prefrontal cortex and mesolimbic dopamine systems, the hippocampus demonstrates a protracted development through adolescence. Here, we propose that developmental trajectories of the hippocampus and hippocampal-prefrontal (HPC-PFC) interactions support the integration and organization of experiences that can influence prefrontal systems. First, we will present our model where we propose that adolescence is a period of specialization in which the maturation of relevant brain systems peaks. This in turn allows the critical integration of relevant brain processes across the hippocampus and prefrontal cortex that lead to the stabilization of cognition in adulthood. Specifically, we will present brain structural evidence that hippocampal memory and prefrontal executive systems have reached critical levels of maturation and that HPC-PFC interactions strengthen in adolescence. We will then present neurobehavioral evidence that the ability to use prior experiences to facilitate goal-relevant behavior, i.e. the execution of task-relevant demands, is enhanced through adolescence. Finally, we expand upon prior models of interactions between executive and reward systems to provide a mechanistic role for the dopaminergic system in supporting these developmental trajectories. Specifically, we predict that peaks in dopaminergic signaling, which occur in adolescence, not only expand memories of prior experiences, but also promote HPC-PFC interactions to incorporate these prior experiences to support task-relevant behavior. We believe these mechanisms support the ability for adolescents to actively acquire experiences from their environment and prioritize experiences that will continue to support goal-oriented behavior throughout adulthood.
Section snippets
A model for integration of prior experience to support adaptive behavior in adolescence
In this review, we build upon prior neurodevelopmental models to include the role of information gathering and episodic memory in the maturation and refinement of executive function. Previous models have proposed that executive functions in adolescents are undermined by significant immaturities in prefrontal systems in addition to a hyperactive motivational drive (Shulman et al., 2016, Spear, 2000). We have extended this model to underscore that prefrontal systems have reached a threshold of
Neural systems underlying the integration of prior experience and executive function
Our model proposes that adolescence represents a time when individuals retrieve acquired experiences to inform task-relevant behavior by extracting information from relevant, previous episodes. This ability becomes relevant when individuals have to inform their current behavioral responses based on information learned in the past. For example, a teen may hesitantly walk into a party at a new place not knowing what to expect. However, when she sees friends she has partied with in the past, she
Structural development of integrated hippocampal-prefrontal circuitry
Our model postulates that the ability for retrieval of relevant prior experience to support task-relevant behavior emerges through the development of integrated HPC-PFC circuitry. In support of this model is a substantial and growing body of work demonstrating structural development within and between the hippocampus and prefrontal cortex. This circuit includes some of the most protracted structural changes that have been observed in the developing brain and includes changes not only in the
Neurobehavioral evidence of the refinement of integrated hippocampal-prefrontal function throughout adolescence
In the prior section, we provided evidence for structural integration across HPC-PFC circuits throughout adolescence. The structural development of these integrated circuits is paralleled by developmental improvements in the ability to reliably extract information from relevant prior experiences in service of task-related behaviors. This is evidenced both by neuroimaging investigations of facilitations in integrated HPC-PFC function as well as behavioral studies indicating a refinement of
A role for dopaminergic neuromodulation in guiding the maturation of integrated hippocampal-prefrontal function throughout adolescence
Thus far, we have provided evidence for the development of distributed information processing throughout the prefrontal cortex and hippocampus throughout adolescence, which is associated with the ability to effectively retrieve relevant prior experiences in service of task-relevant behavior. Open questions remain, however, as to why the neurodevelopment of this circuit is particularly sensitive to adolescence. Although not directly tested in a neurodevelopmental framework, we theorize that
Conclusions
Adolescence is a time characterized by heightened sensation-seeking and a newly acquired access to prefrontal executive function that motivates exploration and experience gathering. We introduce the Experience-Driven Adaptive Cognitive Model of adolescence that integrates the retrieval of relevant prior experiences with refinement in prefrontal executive function. Together, this integration may underlie the ability to establish adaptive heuristics critical for adult level functioning. We
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