Neurodevelopmental trajectories of the human cerebral cortex

Abstract

Understanding the organization of the cerebral cortex remains a central focus of neuroscience. Cortical maps have relied almost exclusively on the examination of postmortem tissue to construct structural, architectonic maps. These maps have invariably distinguished between areas with fewer discernable layers, which have a less complex overall pattern of lamination and lack an internal granular layer, and those with more complex laminar architecture. The former includes several agranular limbic areas, and the latter includes the homotypical and granular areas of association and sensory cortex. Here, we relate these traditional maps to developmental data from noninvasive neuroimaging. Changes in cortical thickness were determined in vivo from 764 neuroanatomic magnetic resonance images acquired longitudinally from 375 typically developing children and young adults. We find differing levels of complexity of cortical growth across the cerebrum, which align closely with established architectonic maps. Cortical regions with simple laminar architecture, including most limbic areas, predominantly show simpler growth trajectories. These areas have clearly identified homologues in all mammalian brains and thus likely evolved in early mammals. In contrast, polysensory and high-order association areas of cortex, the most complex areas in terms of their laminar architecture, also have the most complex developmental trajectories. Some of these areas are unique to, or dramatically expanded in primates, lending an evolutionary significance to the findings. Furthermore, by mapping a key characteristic of these development trajectories (the age of attaining peak cortical thickness) we document the dynamic, heterochronous maturation of the cerebral cortex through time lapse sequences ("movies").

Figure 1.

The age distribution of the data. The age at each scan is indicated by a blue diamond. For each subject, the first scan is always the leftmost; subjects with repeated scans have a horizontal line drawn connecting the age at first scan with the age at later scans.

Figure 2.

Complexity of developmental trajectories throughout the cerebral cortex. The brain maps show the vertices having a cubic (red), quadratic (green) or linear (blue) developmental trajectory. The graphs show the growth pattern for each of these divisions. In order there are dorsal, right lateral, left medial, left lateral, and right medial views. The corpus callosum is blacked out.

Figure 3.

Graphs showing raw cortical thickness data in blue, with the fitted trajectory superimposed in pink. a–c, The first three images show in order the mean cortical thickness and trajectory for representative regions: the superior frontal gyri, which have a cubic trajectory (a); the portion of the insula which has a quadratic trajectory, seen in green in Figure 5 (b); the portion of the orbitofrontal cortex which has a linear trajectory, seen in blue in Figure 4 (c).

Figure 4.

A, Complexity of developmental trajectories throughout the orbitofrontal cortex, projected onto a standard brain template. The anterior and lateral orbitofrontal cortex has a cubic fit (red); medial and posterior orbitofrontal cortex has simpler quadratic (green) and linear (blue) trajectories. B, The trajectories are superimposed on a cytoarchitectonic map of the region by Öngür et al. (2003) to illustrate the overlap between the cytoarchitectonic fields and regional differences in trajectories. C, The trajectory of each of the divisions.

Figure 5.

Top, Detailed views of trajectories in the right medial prefrontal cortex, where isocortical regions have a cubic trajectory, and transitional areas have either a quadratic trajectory (e.g., the agranular and poorly laminated cortex of area 24a in the cingulate gyrus) or a linear decline in thickness (e.g., the thin and largely agranular cortex of the gyrus rectus). Bottom, The right insula shows progressively more complex trajectories moving: the posterior portion has a cubic trajectory (red), the body of the insula has a quadratic fit (green) and the anterior insula has a linear fit (blue). A similar pattern holds for the left insula.

Figure 6.

Age of attaining peak cortical thickness across the cerebral cortex. Peak thickness can only be estimated for regions with a cubic or quadratic trajectory and not for regions with linear change (which are indicated with a darker red shade). The changes are illustrated dynamically in supplemental Movies 1 and 2, available at www.jneurosci.org as supplemental material.