Review article
The role of experience in adolescent cognitive development: Integration of executive, memory, and mesolimbic systems

https://doi.org/10.1016/j.neubiorev.2016.07.034Get rights and content

Highlights

  • Retrieval of relevant prior experience can facilitate executive function.

  • Adolescents refine the ability to integrate prior experience to support task behavior.

  • Hippocampal-prefrontal integration continues to mature throughout adolescence.

  • Dopamine signaling during adolescence may support hippocampal-prefrontal integration.

Abstract

Adolescence marks a time of unique neurocognitive development, in which executive functions reach adult levels of maturation. While many core facets of executive function may reach maturation in childhood, these processes continue to be refined and stabilized during adolescence. We propose that this is mediated, in part, by interactions between the hippocampus and prefrontal cortex. Specifically, we propose that development of this circuit refines adolescents’ ability to extract relevant information from prior experience to support task-relevant behavior. In support of this model, we review evidence for protracted structural and functional development both within and across the hippocampus and prefrontal cortex. We describe emerging research demonstrating the refinement of adolescents’ ability to integrate prior experiences to support goal-oriented behavior, which parallel hippocampal-prefrontal integration. Finally, we speculate that the development of this circuit is mediated by increases in dopaminergic neuromodulation present in adolescence, which may underlie memory processing, plasticity, and circuit integration. This model provides a novel characterization of how memory and executive systems integrate throughout adolescence to support adaptive behavior.

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

References (144)

  • R.A. Diana et al.

    Imaging recollection and familiarity in the medial temporal lobe: a three-component model

    Trends Cogn. Sci.

    (2007)
  • B.B. Doll et al.

    The ubiquity of model-based reinforcement learning

    Curr. Opin. Neurobiol.

    (2012)
  • B.B. Doll et al.

    Multiple memory systems as substrates for multiple decision systems

    Neurobiol. Learn. Mem.

    (2015)
  • D. Durstewitz et al.

    The computational role of dopamine D1 receptors in working memory

    Neural Net.

    (2002)
  • M.F. Eckenhoff et al.

    A quantitative analysis of synaptogenesis in the molecular layer of the dentate gyrus in the rhesus monkey

    Brain Res. Dev. Brain Res.

    (1991)
  • A.S. Finn et al.

    Developmental dissociation between the maturation of procedural memory and declarative memory

    J. Exp. Child Psychol.

    (2016)
  • S. Ghetti et al.

    Neural changes underlying the development of episodic memory during middle childhood

    Dev. Cogn. Neurosci.

    (2012)
  • S. Gluth et al.

    Effective connectivity between hippocampus and ventromedial prefrontal cortex controls preferential choices from memory

    Neuron

    (2015)
  • H. Gurden et al.

    Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal cortex long-term potentiation

    Neuroscience

    (1999)
  • S.A. Gutnikov et al.

    Monkeys can associate visual stimuli with reward delayed by 1s even after perirhinal cortex ablation, uncinate fascicle section or amygdalectomy

    Behav. Brain Res.

    (1997)
  • C.A. Hartley et al.

    The neuroscience of adolescent decision-making

    Curr. Opin. Behav. Sci.

    (2015)
  • K.M. Hasan et al.

    Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography

    Brain Res.

    (2009)
  • P.S. Hunt et al.

    Adolescent transitions in reflexive and non-reflexive behavior: review of fear conditoninig and impulse control in rodent models

    Neurosci. Biobehav. Rev.

    (2016)
  • J.B. Hutchinson et al.

    Memory-guided attention: control from multiple memory systems

    Trends Cogn. Sci.

    (2012)
  • S. Ikemoto et al.

    The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking

    Brain Res. Brain Res. Rev.

    (1999)
  • T.M. Jay

    Dopamine: a potential substrate for synaptic plasticity and memory mechanisms

    Prog. Neurobiol.

    (2003)
  • D. Kumaran et al.

    Tracking the emergence of conceptual knowledge during human decision making

    Neuron

    (2009)
  • Y. Kwak et al.

    The rational adolescent: strategic information processing during decision making revealed by eye tracking

    Cogn. Dev.

    (2015)
  • C. Lebel et al.

    Diffusion tensor imaging of white matter tract evolution over the lifespan

    Neuroimage

    (2012)
  • J.K. Lee et al.

    Volume of hippocampal subfields and episodic memory in childhood and adolescence

    NeuroImage

    (2014)
  • J.E. Lisman et al.

    The hippocampal-VTA loop: controlling the entry of information into long-term memory

    Neuron

    (2005)
  • S.Z. Meng et al.

    Developmental and age-related changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia

    Brain Res.

    (1999)
  • V. Menon et al.

    Maturation of medial temporal lobe response and connectivity during memory encoding

    Brain Res. Cogn. Brain Res.

    (2005)
  • T. Meulemans et al.

    Implicit sequence learning in children

    J. Exp. Child Psychol.

    (1998)
  • V.P. Murty et al.

    fMRI studies of successful emotional memory encoding: a quantitative meta-analysis

    Neuropsychologia

    (2010)
  • S.L. Andersen et al.

    Developmental differences in dopamine synthesis inhibition by (+/−)-7-OH-DPAT

    Naunyn-Schmiedeberg’s Arch. Pharmacol.

    (1997)
  • F. Bähner et al.

    Hippocampal-dorsolateral prefrontal coupling as a species-conserved cognitive mechanism: a human translational imaging study

    Neuropsychopharmacology

    (2015)
  • S. Bao et al.

    Cortical remodelling induced by activity of ventral tegmental dopamine neurons

    Nature

    (2001)
  • H. Barbas et al.

    Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey

    Hippocampus

    (1995)
  • N. Barnea-Goraly et al.

    White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study

    Cereb. Cortex

    (2005)
  • F.M. Benes et al.

    Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood

    Arch. Gen. Psychiatry

    (1994)
  • F.M. Benes

    Myelination of cortical-hippocampal relays during late adolescence

    Schizophr. Bull.

    (1989)
  • R.S. Blumenfeld et al.

    Prefrontal cortex and long-term memory encoding: an integrative review of findings from neuropsychology and neuroimaging

    Neuroscientist

    (2007)
  • G. Borst et al.

    Inhibition of misleading heuristics as a core mechanism for typical cognitive development: evidence from behavioural and brain-imaging studies

    Dev. Med. Child Neurol.

    (2015)
  • C.J. Brainerd et al.

    Behavioral measurement of remembering phenomenologies: so simple a child can do it

    Child Dev.

    (2004)
  • T.J. Bussey et al.

    Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning

    Behav. Neurosci.

    (2002)
  • C. Cavada et al.

    The anatomical connections of the macaque monkey orbitofrontal cortex. A review

    Cereb. Cortex

    (2000)
  • E. Cocchi et al.

    Hippocampal pruning as a new theory of schizophrenia etiopathogenesis

    Mol. Neurobiol.

    (2016)
  • R.E. Dahl

    Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address

    Ann. N. Y. Acad. Sci.

    (2004)
  • A.M. Daugherty et al.

    Age differences in hippocampal subfield volumes from childhood to late adulthood

    Hippocampus

    (2016)
  • Cited by (0)

    View full text