Sustained attention and prediction: distinct brain maturation trajectories during adolescence.

Alix Thillay,Valérie Gissot,Isabelle Carteau-Martin,Aurélie Bidet-Caulet,Frédérique Bonnet-Brilhault,Sylvie Roux,Robert T Knight

doi:10.3389/fnhum.2015.00519

Abstract

Adolescence is a key period for frontal cortex maturation necessary for the development of cognitive ability. Sustained attention and prediction are cognitive functions critical for optimizing sensory processing, and essential to efficiently adapt behaviors in an ever-changing world. The aim of the current study was to investigate the brain developmental trajectories of attentive and predictive processing through adolescence. We recorded EEG in 36 participants from the age of 12–24 years (three age groups: 12–14, 14–17, 18–24 years) to target development during early and late adolescence, and early adulthood. We chose a visual target detection task which loaded upon sustained attention, and we manipulated target predictability. Continued maturation of sustained attention after age 12 was evidenced by improved performance (hits, false alarms (FAs) and sensitivity) in a detection task, associated with a frontal shift in the scalp topographies of the Contingent Negative Variation (CNV) and P3 responses, with increasing age. No effect of age was observed on predictive processing, with all ages showing similar benefits in reaction time, increases in P3 amplitude (indexing predictive value encoding and memorization), increases in CNV amplitude (corresponding to prediction implementation) and reduction in target-P3 latency (reflecting successful prediction building and use), with increased predictive content. This suggests that adolescents extracted and used predictive information to generate predictions as well as adults. The present results show that predictive and attentive processing follow distinct brain developmental trajectories: prediction abilities seem mature by the age of 12 and sustained attention continues to improve after 12-years of age and is associated with maturational changes in the frontal cortices.

Highlights

The optimization of sensory processing by the brain, a limited-capacity system, is a key function that alleviates the burden of sensory information to be processed
Post hoc analyses revealed that 12–14 year-olds detected less random target (randT) and made more false alarm (FA) than 18–24 year-olds (p = 0.018 or p = 0.001, respectively), and presented a smaller d compared to 14–17 yearolds and 18–24 year-olds (p = 0.011 and p = 0.003, respectively)
Continued maturation of sustained attention after age 12 was evidenced by improved performance in a detection task and a frontal shift in P3 and Contingent Negative Variation (CNV) topographies with increasing age

Summary

Introduction

The optimization of sensory processing by the brain, a limited-capacity system, is a key function that alleviates the burden of sensory information to be processed. This optimization is enabled by two complementary processes: (1) attention which prioritizes sensory processing according to task-relevance (Sarter et al, 2001); (2) prediction which facilitates perception based on prior likelihood (Summerfield and Egner, 2009). Predictive processing is far from being a unitary function and comprises several mechanisms such as the generation of prediction based on encoding and memorization of predictive information, and the implementation of prediction via the deployment of preparatory mechanisms resulting in facilitated processing of upcoming events and optimized behaviors. Sustained attention and prediction are essential to efficiently adapt behaviors in an ever-changing world and support ‘‘proactive’’ control defined as sustained preparatory mechanisms for upcoming events according to the Dual Mechanisms of Control framework (Braver, 2012)

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Conclusion