Adjusting behavior to changing environmental demands with development

Highlights

• Plasticity is the capacity to adapt to changing environmental demands.

• Environmental demands change with development, especially during adolescence.

• The prefrontal cortex is involved in flexibly adjusting behavior to changing demands.

• Reward regions can render the prefrontal cortex unable to flexibly modulate behavior.

• Biological constraints and experiential history shape our behavioral flexibility.

Abstract

Plasticity refers to changes in the brain that enable an organism to adapt its behavior in the face of changing environmental demands. The evolutionary role of plasticity is to provide the cognitive flexibility to learn from experiences, to monitor the world based on learned predictions, and adjust actions when these predictions are violated. Both progressive (myelination) and regressive (synaptic pruning) brain changes support this type of adaptation. Experience-driven changes in neural connections underlie the ability to learn and update thoughts and behaviors throughout life. Many cognitive and behavioral indices exhibit nonlinear life-span trajectories, suggesting the existence of specific sensitive developmental periods of heightened plasticity. We propose that age-related differences in learning capabilities and behavioral performance reflect the distinct maturational timetable of subcortical learning systems and modulatory prefrontal regions. We focus specifically on the developmental transition of adolescence, during which individuals experience difficulty flexibly adjusting their behavior when confronted with unexpected and emotionally salient events. In this article, we review the findings illustrating this phenomenon and how they vary by individual.

Introduction

One of the fundamental purposes of brain plasticity is to provide the capacity to adapt and optimize behavior in accordance with the current environmental demands. This capability to learn through experience to obtain reward or to avoid danger serves a clear evolutionary purpose. An organism's fitness may critically depend on the ability to adjust behavior to maximize the likelihood of a successful hunt or, more contemporarily, a lucrative business deal. Subcortical systems have been shown to support essential, evolutionarily-conserved learning processes involving reward (Galvan et al., 2005, Pagnoni et al., 2002, Schultz et al., 1997) and threat (Delgado et al., 2008, Soliman et al., 2010). But these systems do not operate independently; rather they are part of a broad interactive network of brain regions (Casey et al., 2001). Regions of prefrontal cortex are thought to play a modulatory role within this network, by enabling the suppression of the subcortical regions involved in immediate motivationally-driven behaviors in favor of longer term goal-oriented ones (for a review, see (Somerville and Casey, 2010).

The ability to adapt and optimize behavior varies as a function of age, the individual, as well as context. Age-related differences in cognitive flexibility may arise due to both maturational constraints of developing brain regions (Galvan et al., 2006), and the connectivity between interacting brain systems (Liston et al., 2006). These differences are particularly apparent during transitional periods, when previously adaptive behaviors may gradually become incompatible with a new range of experiences that arise across the lifespan. Flexibility in adjusting behavior to changing environmental demands also depends upon an individual‘s unique experiential history. As such, some individuals are less able than others to flexibly suppress an inappropriate action, such as not eating cookies when dieting. That flexibility is particularly challenged in the context of highly salient cues (e.g., an ice cream sundae). This paper examines flexibility and rigidity in behavioral adaptation as environmental demands vary across development and individuals.