Fetal Gyrification in Cynomolgus Monkeys: A Concept of Developmental Stages of Gyrification

Abstract

Our article summarizes a series of studies about fetal gyrification and its relation to cerebral growth in cynomolgus monkeys. Based on the cerebral growth (i.e., brain weight, cerebral volume, and frontooccipital length of the cerebral hemisphere) and the developmental pattern of gyrification in each sulcus of cynomolgus monkeys, we divided the gyrification process into four stages: Stage 1. Demarcation of cerebral lobes and limbic gyri; Stage 2. Demarcation of neocortical gyri; Stage 3. Emergence of secondary and tertiary sulci; and Stage 4. Growth of sulcal length and depth. Each stage of those gyrification processes was influenced by different developmental events, such as the emergence of corticocortical long-associative fiber tracts, cortical maturations, and subcortical white-matter development. This is the first report to systematically propose gyrification processes closely related to the order of phyologenetical development of the cerebral cortex in primates.

Conical expansion of the outer subventricular zone and the role of neocortical folding in evolution and development

“…3D reconstructions of fetal human brains from Barnette et al (2009). Figure follows Sawada et al (2012b). …”

“…The correlative increase in cerebral volume and gyrification during this stage, including a dramatic increase in gyri in the occipital region, may in fact constitute the formation of a characteristic pattern of gyrencephaly common to all gyrencephalic primates. Work in Old World monkeys has shown that all neocortical gyri, with the exception of the superior temporal gyrus, emerge during Stage 1 and that both the chronology of emergence and rostrocaudal distribution of gyri are homologous in monkeys and humans (Zilles et al, 1988; Rilling and Insel, 1999; Sawada et al, 2012a,b). There is, despite this broad conservation, a delayed emergence of the parietoccipital gyri (e.g., cuneus, angular gyrus, supramarginal gyrus) in humans compared to monkeys, which, because these gyri are associated with Wernicke's area in humans but dorsal extrastriate cortex in monkeys (Sawada et al, 2012a,b), may indicate that heterochronic changes in gyri emergence reflect species-specific adaptations in particular cortical regions.…”

Cortical Folding of the Primate Brain: An Interdisciplinary Examination of the Genetic Architecture, Modularity, and Evolvability of a Significant Neurological Trait in Pedigreed Baboons (GenusPapio)

“…Restricting phenotypic variance into modules also allows systems to evolve patterns of correlation that facilitate future alteration of evolutionary traits through the convergence of genetic and functional modules (Cheverud 1996;Wagner 1996). The similarity of variation structure in genetic and phenotypic matrices thus illustrates the selective grouping of traits into related units in these two domains, providing a ready framework for future adaptive morphological change and an evolutionarily beneficial situation of increased morphological integration for traits that need to be functionally compatible with one another in an organism's life.The similarity in matrix variation structure between the anatomical location of the sulci and the day on which the sulcus first emerges during development parallels ontogenetic findings that the brain typically develops the primary and most deep-set folds first during development, with secondary folds developing next, and superficial wrinkles and projections off of the primary folds developing last (Huang et al 2009;Sawada et al 2012). The bulk of the primary folds are located toward the central region of the brain (lf, sts, cs), followed by the back of the brain (lu, ips), and finally the frontal folds (ps, spcd, iar).…”

“…Based on embryonic day of emergence of each landmark sulci. Created from data presented in Sawada et al (2012).…”

“…As the raw matrix was not symmetric due to differences between numbers of axons projecting from source to target vs. from target to source, a compromise matrix of the average between these two measures was used. Some regions were characterized only as an axon source and not a target, in which case this measure alone was used in downstream analyses.A developmental matrix was created from data published by Sawada et al (2012) illustrating the ontogeny of cortical development in M. fascicularis (Sawada et al 2012) (Table S7).We created a distance matrix between sulci based on their relative times of developmental emergence in days from conception. Sulci emerge between embryonic days 70 and 135.…”