Development of the Cerebral Cortex across Adolescence: A Multisample Study of Inter-Related Longitudinal Changes in Cortical Volume, Surface Area, and Thickness

Abstract

Before we can assess and interpret how developmental changes in human brain structure relate to cognition, affect, and motivation, and how these processes are perturbed in clinical or at-risk populations, we must first precisely understand typical brain development and how changes in different structural components relate to each other. We conducted a multisample magnetic resonance imaging study to investigate the development of cortical volume, surface area, and thickness, as well as their inter-relationships, from late childhood to early adulthood (7–29 years) using four separate longitudinal samples including 388 participants and 854 total scans. These independent datasets were processed and quality-controlled using the same methods, but analyzed separately to study the replicability of the results across sample and image-acquisition characteristics. The results consistently showed widespread and regionally variable nonlinear decreases in cortical volume and thickness and comparably smaller steady decreases in surface area. Further, the dominant contributor to cortical volume reductions during adolescence was thinning. Finally, complex regional and topological patterns of associations between changes in surface area and thickness were observed. Positive relationships were seen in sulcal regions in prefrontal and temporal cortices, while negative relationships were seen mainly in gyral regions in more posterior cortices. Collectively, these results help resolve previous inconsistencies regarding the structural development of the cerebral cortex from childhood to adulthood, and provide novel insight into how changes in the different dimensions of the cortex in this period of life are inter-related.SIGNIFICANCE STATEMENT Different measures of brain anatomy develop differently across adolescence. Their precise trajectories and how they relate to each other throughout development are important to know if we are to fully understand both typical development and disorders involving aberrant brain development. However, our understanding of such trajectories and relationships is still incomplete. To provide accurate characterizations of how different measures of cortical structure develop, we performed an MRI investigation across four independent datasets. The most profound anatomical change in the cortex during adolescence was thinning, with the largest decreases observed in the parietal lobe. There were complex regional patterns of associations between changes in surface area and thickness, with positive relationships seen in sulcal regions in prefrontal and temporal cortices, and negative relationships seen mainly in gyral regions in more posterior cortices.

Charting shared developmental trajectories of cortical thickness and structural connectivity in childhood and adolescence

“…Regional modelling of cortical thickness has found similar patterns, broadly respecting the organisational hierarchy of the cortex (Fjell et al, 2015;Tamnes et al, 2010Tamnes et al, , 2017Vijayakumar et al, 2016). Regional modelling of cortical thickness has found similar patterns, broadly respecting the organisational hierarchy of the cortex (Fjell et al, 2015;Tamnes et al, 2010Tamnes et al, , 2017Vijayakumar et al, 2016).…”

A three‐wave longitudinal study of subcortical–cortical resting‐state connectivity in adolescence: Testing age‐ and puberty‐related changes

“…It is particularly relevant to consider these transformations not only in relation to neural structural or localized activation changes, but also in relation to functional connectivity changes in the adolescent brain (Casey, ; Crone & Dahl, ; Stevens, ). Relative to studies examining structural (Tamnes et al, ) and functional (Telzer et al, ) brain development, very few studies have examined longitudinal functional connectivity changes. The goal of this study was therefore to analyze within and between subcortical–cortical connectivity in participants ages 8–29 years, using a three‐wave longitudinal design covering 5 years for each individual.…”

Emerging depression in adolescence coincides with accelerated frontal cortical thinning

“…Nonetheless, one central process is presumed to be intracortical myelination (Grydeland, Walhovd, Tamnes, Westlye, & Fjell, ; Whitaker et al., ). Furthermore, the distinct components of cortical morphology, thickness, and surface area show different developmental trajectories (Tamnes et al., ; Wierenga, Langen, Oranje, & Durston, ).…”