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.T he human cerebral cortex is characterized by regional nonuniformities in cellular structure that change with age. Near term, there are regional variations in synaptic density (1, 2), dendritic length, and dendritic spine density (3). Postnatally, synaptic density increases dramatically, reaches a peak density in early childhood, and then undergoes synaptic pruning with a 2-fold or greater reduction (4). The time course of these synaptic changes differs across regions, with primary sensory areas attaining peak density and adult levels earlier than higher order "association" areas (2, 5). In adults, there are large regional nonuniformities in neuronal density (6), dendritic size, branching complexity, and spine density (7).This evidence for cellular nonuniformities provides grounds for anticipating regional differences in macroscopic aspects of postnatal cortical maturation. Indeed, studies of gray matter volume and overall brain growth provide evidence for complex regional patterns of morphological change during childhood and adolescence (8, 9). We recently used a surface-based approach to compare cortical structure in human term infants to adults. That analysis suggested that although many adult cortical shape characteristics are well established at birth, there may be regional differences in the maturity of cortical folding in term infants compared with adults (10).Comparisons with nonhuman primates, especially the intensively studied macaque monkey, provide another basis for evaluating regional differences in cortical maturation. Since the evolutionary divergence between humans and macaques ∼25 million years ago (11), cortical expansion has been far greater in human lineage than in the macaque lineage. Compared with the macaque cortex, the human c...

Relaxed genetic control of cortical organization in human brains compared with chimpanzees

“…Those sulcal dimensions still show substantially lower heritability in humans than do the developmentally and evolutionarily primary sulci such as the central sulcus and the Sylvian fissure. Studies of cortical development in humans have shown differential regional enlargement, which has been suggested to reflect extended maturation and complexity of dendritic and synaptic architecture in association areas (24). Lateral temporal, lateral parietal, and dorsal and medial prefrontal regions show the greatest degree of expansion from birth to adulthood, and it has been suggested that cortical circuits in these regions may be more sensitive to postnatal experience (24).…”

“…Studies of cortical development in humans have shown differential regional enlargement, which has been suggested to reflect extended maturation and complexity of dendritic and synaptic architecture in association areas (24). Lateral temporal, lateral parietal, and dorsal and medial prefrontal regions show the greatest degree of expansion from birth to adulthood, and it has been suggested that cortical circuits in these regions may be more sensitive to postnatal experience (24). Heritability patterns observed in chimpanzees and humans in the present study are consistent with the proposition that humans have evolved relaxed genetic control on cortical organization, especially in areas related to higher-order cognitive functions.…”

Large-Scale Gradients in Human Cortical Organization

“…For example, transmodal regions of the DMN, although located at distant points of the rostrocaudal axis, have similar gene expression patterns. These regions also show protracted developmental expansion and maturation in humans [63]. While much remains to be learned about neurodevelopmental gradients in the human cerebral cortex, such research can help to integrate observations across different cortical features and establish an informed developmental basis for the proposed intrinsic coordinate system.…”

Parcellations and Connectivity Patterns in Human and Macaque Cerebral Cortex

“…This approach provides evidence of hotspots of human evolution in lateral temporal, parietal, and prefrontal cortex that have expanded dramatically in the human lineage relative to that in the macaque; the pattern is remarkably similar to human postnatal cortical expansion, between birth and adulthood (Van Essen and Dierker 2007;Hill et al 2010). To better understand this pattern of evolutionary divergence, it is desirable to have a larger set of known or presumed homologies between specie, and also to have improved methods of interspecies registration that handle the highly nonuniform spatial patterns of expansion.…”

“…2 Group-average myelin maps for macaque (n ¼ 19, Yerkes19) and human (n ¼ 196, HCP), adapted from Glasser et al (2013a. Myelin maps were generated by computing the T1w/T2w ratio for each cortical gray matter voxel, mapping it to individual cortical surfaces, and registering the individuals to a species-specific atlas surface (Glasser and Van Essen 2011) using the MSM registration method myelinated higher cognitive regions, whereas the least expansion (~2-fold) occurs in early sensory areas (Hill et al 2010). A likely cellular-level correlate is that, in the macaque, dendritic arbors sizes and synapse number increase between birth and adulthood in inferotemporal cortex, whereas there is a net decrease in both measures for early visual areas (Elston et al 2010).…”