Similar patterns of cortical expansion during human development and evolution

Abstract

The cerebral cortex of the human infant at term is complexly folded in a similar fashion to adult cortex but has only one third the total surface area. By comparing 12 healthy infants born at term with 12 healthy young adults, we demonstrate that postnatal cortical expansion is strikingly nonuniform: regions of lateral temporal, parietal, and frontal cortex expand nearly twice as much as other regions in the insular and medial occipital cortex. This differential postnatal expansion may reflect regional differences in the maturity of dendritic and synaptic architecture at birth and/or in the complexity of dendritic and synaptic architecture in adults. This expression may also be associated with differential sensitivity of cortical circuits to childhood experience and insults. By comparing human and macaque monkey cerebral cortex, we infer that the pattern of human evolutionary expansion is remarkably similar to the pattern of human postnatal expansion. To account for this correspondence, we hypothesize that it is beneficial for regions of recent evolutionary expansion to remain less mature at birth, perhaps to increase the influence of postnatal experience on the development of these regions or to focus prenatal resources on regions most important for early survival.

Fig. 1.

Postnatal cortical surface expansion. Maps of postnatal cortical surface expansion on the standard mesh average inflated term infant surfaces for both hemispheres, shown in lateral (A), medial (B), dorsal (C), and ventral (D) views. The absolute expansion scale indicates how many times larger the surface area of a given region is in adulthood relative to that region’s area at term. The relative expansion scale indicates the difference in proportion of total surface area at term birth and adulthood.

Fig. 2.

Statistically significant clusters of nonuniform postnatal cortical surface expansion. Significant clusters for right (A) and left (B) hemispheres. White contours enclose regions occupying a significantly smaller proportion of the cortex in adulthood than at term. Black contours enclose regions occupying a significantly larger proportion of the cortex in adulthood than at term. (C) Statistically significant clusters detected by interhemipsheric symmetry testing.

Fig. 3.

Individual folding patterns in term infants and adults for regions of high and low postnatal expansion. Individual standard-mesh fiducial surfaces for high-expanding lateral temporal cortex (A–C) and low-expanding medial temporal/occipital cortex (D–F). White boxes at top show the approximate region being analyzed. For each region, term infant surfaces are shown in the left column of panels, and adult surfaces are shown in the right column of panels.

Fig. 4.

Comparison of evolutionary and postnatal cortical surface expansion. (A) Map of regional evolutionary cortical expansion between an adult macaque and the average human adult PALS-B12 atlas (right hemisphere only). Evolution expansion scale indicates how many times larger the surface area is in humans relative to the corresponding area in the macaque. (B) Map of human postnatal cortical expansion (combined left and right hemispheres) for comparison (detailed in Fig. 1 legend). (C) Correlation map comparing postnatal to evolutionary cortical surface expansion.

Fig. 5.

ROIs mapped to the result of postnatal cortical expansion. (A) Postnatal surface expansion map (combined left and right hemispheres) overlaid with ROIs from human and macaque studies. Black outlines identify ROIs from studies in humans. Colored spheres indicate ROIs from studies in macaque monkeys. (B) Similar views of the F99 macaque atlas labeled with the macaque ROIs from the top panel indicating the homologous location on the macaque. 10, Brodmann area 10; 21, Brodmann area 21; FEF, frontal eve fields; HG, Heschl's gyrus; LIPv, ventral part of lateral intraparietal cortex; MFG, anterior third of the middle frontal gyrus; MT, medial temporal visual region; PFC, prefrontal cortex; STPp, visual region on anterior bank of superior temporal sulcus; TEa, visual region on the posterior bank of the superior temporal sulcus; TEpd, visual region on the inferior temporal gyrus; V1, primary visual cortex; V2, secondary visual cortex. References for studies used to identify regions of interest: V1, MT, TEa (58); V2, LIP, MT 7a (59); FEF (28); TEpd, PFC (23).