Evo-devo and the primate isocortex: the central organizing role of intrinsic gradients of neurogenesis

Abstract

Spatial gradients in the initiation and termination of basic processes, such as cytogenesis, cell-type specification and dendritic maturation, are ubiquitous in developing nervous systems. Such gradients can produce a niche adaptation in a particular species. For example, the high density of photoreceptors and neurons in the 'area centralis' of some vertebrate retinas result from the early maturation of its center relative to its periphery. Across species, regularities in allometric scaling of brain regions can derive from conserved spatial gradients: longer neurogenesis in the alar versus the basal plate of the neural tube is associated with relatively greater expansion of alar plate derivatives in larger brains. We describe gradients of neurogenesis within the isocortex and their effects on adult cytoarchitecture within and across species. Longer duration of neurogenesis in the caudal isocortex is associated with increased neuron number and density per column relative to the rostral isocortex. Later-maturing features of single neurons, such as soma size and dendritic spine numbers reflect this gradient. Considering rodents and primates, the longer the duration of isocortical neurogenesis in each species, the greater the rostral-to-caudal difference in neuron number and density per column. Extended developmental duration produces substantial, predictable changes in the architecture of the isocortex in larger brains, and presumably a progressively changed functional organization, the properties of which we do not yet fully understand. Many features of isocortical architecture previously viewed as species- or niche-specific adaptations can now be integrated as the natural outcomes of spatiotemporal gradients that are deployed in larger brains.

Figure 1

The difference in terminal neurogenesis between the anterior (i.e., primary somatosensory cortex, S1) and posterior cortex (i.e., primary visual cortex, V1) is regressed against the natural-logged values (Ln) of developmental duration in eutherian mammalian species. The translating time model predicts that as overall developmental schedules lengthen, the difference in the duration of terminal neurogenesis across the presumptive isocortical axis increases.

Figure 2

Neuron numbers per unit of cortical surface area in an owl monkey (Aotus trivirgatus) and in a hamster (Mesocricetus auratus). Neuron numbers per unit of cortical surface area increase from the frontal to the parieto-occipital cortex in the owl monkey but this systematic variation is not clear in the smaller brained hamster.

Figure 3

Layer II/III neuronal soma size plotted against the rostro-caudal axis of the isocortex in three species of New World monkeys. These data show that as overall isocortical neuron numbers increase (i.e., layer II-VI neuron numbers), the discrepancy between layer II/III neuronal soma size between the frontal and parieto-occipital cortex increases in these taxa. These data are from Cahalane et al., 2012 and Charvet et al., 2013.

Figure 4

Estimated total number of spine in layer III pyramidal neurons in prefrontal, temporal and occipital regions in marmosets (8 g), macaque (93.8 g) and a human (1350 g). The difference in total number of spines of layer III pyramidal cells between the frontal and occipital cortex is greater in bigger brains. Most of the variation in total estimated spine numbers is in the frontal pole rather than in the occipital region. These data are from Elston et al., 2001.