Protracted development of executive and mnemonic brain systems underlying working memory in adolescence: A longitudinal fMRI study

Abstract

Working memory (WM), the ability to hold information on-line to guide planned behavior, improves through adolescence in parallel with continued maturation of critical brain systems supporting cognitive control. Initial developmental neuroimaging studies with one or two timepoints have provided important though varied results limiting our understanding of which and how neural systems change during this transition into mature WM. In this study, we leverage functional magnetic resonance imaging (fMRI) longitudinal data spanning up to 9 years in 129 normally developing individuals to identify which systems demonstrate growth changes that accompany improvements in WM performance. We used a memory guided saccade task that allowed us to probe encoding, pure maintenance, and retrieval neural processes of WM. Consistent with prior research, we found that WM performance continued to improve into the early 20's. fMRI region of interest (ROI) analyses revealed developmental (1) increases in sensorimotor-related (encoding/retrieval) activity in visual cortex from childhood through early adulthood that were associated with WM accuracy and (2) decreases in sustained (maintenance) activity in executive regions from childhood through mid-adolescence that were associated with response latency in childhood and early adolescence. Together these results provide compelling evidence that underlying the maturation of WM is a transition from reliance on executive systems to specialized regions related to the domain of mnemonic requirements of the task leading to optimal performance.

Keywords: Brain-behavior; Epochs; Individual differences; Maturation; Stages.

Copyright © 2017. Published by Elsevier Inc.

Figures

Figure 1:

Distribution of ages and scans in study sample. Each point represents a time point; color represents year of study (up to 9) as indicated in the legend. Time points belonging to the same individual are connected by lines.

Figure 2:

Plots showing fMRI activation in visual cortex (VC; BA 17/18) during encoding (left), maintenance (middle), and retrieval (right), highlighting developmental increases during encoding and retrieval into early adulthood. Analyses in longitudinal dataset with ROIs drawn from the cross-sectional dataset. Lines indicates spline model fit (color indicates Brodmann Areas, with gray=17 and black=18, and line type indicates hemisphere, with left=dashed and right=solid). Heat plot beneath highlights developmental stages, with active change occurring during shaded periods.

Figure 3:

Plots showing developmental decreases in fMRI activation during maintenance into mid-late adolescence. Analyses in longitudinal dataset with ROIs drawn from the cross-sectional dataset. Lineplot panels indicate spline fits in separate regions, with line type inside the panels showing hemisphere (left=dashed, right=solid, bilateral=dotted). Heat plot beneath highlights developmental stages, with active change occurring during shaded periods.

Figure 4:

Left: Interaction of precision error and fMRI activation in visual cortex in both right (black) and left (gray) hemispheres during encoding, after controlling for age. Right: Interaction of age and latency with fMRI activation in Anterior Cingulate (gray) and the Left Anterior Insula (black) during maintenance; panels indicate developmental stage (left=child, right=teen, age ranges indicated in text). Analyses in longitudinal dataset with ROIs drawn from the cross-sectional dataset. Solid line indicates spline model fit and dashed lines indicate 1 standard deviation from fit line, derived from bootstrapping.