An integrative model of the maturation of cognitive control

Abstract

Brains systems undergo unique and specific dynamic changes at the cellular, circuit, and systems level that underlie the transition to adult-level cognitive control. We integrate literature from these different levels of analyses to propose a novel model of the brain basis of the development of cognitive control. The ability to consistently exert cognitive control improves into adulthood as the flexible integration of component processes, including inhibitory control, performance monitoring, and working memory, increases. Unique maturational changes in brain structure, supported by interactions between dopaminergic and GABAergic systems, contribute to enhanced network synchronization and an improved signal-to-noise ratio. In turn, these factors facilitate the specialization and strengthening of connectivity in networks supporting the transition to adult levels of cognitive control. This model provides a novel understanding of the adolescent period as an adaptive period of heightened experience-seeking necessary for the specialization of brain systems supporting cognitive control.

Keywords: GABA; cognitive control; development; dopamine; inhibition; networks; performance monitoring; working memory.

Figure 1

Results from a longitudinal study of inhibitory control. (a) The rate of response inhibition failures in an AS task decreased with age, with intersubject variability remaining constant with age. The vertical bar indicates the rate of decrease for individual subjects (males in blue, females in red). (b) Activation in the DLPFC decreased until adolescence, when it reached adult levels, whereas activation in the dACC increased with age through adolescence (p-value significance of an inverse fit from a mixed model). (c) Furthermore, dACC percent signal change during error trials mediated the effect of age on performance. One asterisk indicates significance at p < 0.05, and three asterisks indicate significance at p < 0.001. Abbreviations: AS, antisaccade; dACC, dorsal anterior cingulate cortex; DLPFC, dorsolateral prefrontal cortex. Adapted with permission from Ordaz et al. (2013).

Figure 2

Proposed model of the maturation of cognitive control. At the cellular level (a), DA (red) and GABA (blue) systems undergo dynamic changes throughout adolescence. Maturational neurotransmitter changes lead to increased signal-to-noise ratios, power, and synchrony at the circuit level (b). Gray and black lines represent neural signals from two separate brain regions. These circuit-level changes occur in parallel with systems-level alterations (c) of distributed connectivity patterns (depicted here for successful performance during an inhibitory control task). Ellipses represent components of cognitive control, circles represent brain regions, and lines between them indicate pairwise connections. Line thickness represents connection strength. Circles within overlapping networks represent highly integrative regions (see sidebar, Hubs in Networks). Connections that lead to successful performance are strengthened by adulthood, whereas connections that do not are weakened, pruned, or both. Together, these developmental changes, occurring across multiple levels of brain function, contribute to mature cognitive control behavior (d). Abbreviations: DA, dopamine; GABA, γ-aminobutyric acid.