Developmental duration as an organizer of the evolving mammalian brain: scaling, adaptations, and exceptions.

Abstract

Neurodevelopmental duration plays a central role in the evolution of the retina and neocortex in mammals. In the diurnal primate eye and retina, it is necessary to scale the number of cones versus the number of rods with different exponents to defend their respective functions of spatial acuity and sensitivity in eyes of different sizes. The order of photoreceptor precursor specification, cones specified first, rods second, couples their respective cell numbers at maturity to the kinetics of embryonic stem cell proliferation. Different durations of retinogenesis change the ratio of rods to cones produced so as to defend both functions over a range of eye diameters. In the evolution of nocturnality, the same coupling of photoreceptor specification to neurogenesis is altered to fewer cones and many more rods in nocturnal eyes, by delaying the onset of retinogenesis. Similarly, the neocortex also shows coupling of the specification of laminar position with duration of neurogenesis. Overall, duration of neurogenesis directly predicts neocortex volume in most mammalian clades. In larger brains with longer neocortical neurogenesis, its organization changes progressively, differentiating the frontal pole from the occipital pole in volume of connectivity and number of neurons per unit column. This permits greater, hierarchically organized information abstraction with increasing neocortex volume. Exceptions do exist, however, in species of three separate taxa, marsupials, naked mole rats, and bats, which break the correlation of neurodevelopmental duration and brain size. Naked mole rats and bats both have small brains and unusual longevity, coupled with neurodevelopmental periods characteristic of much bigger-brained animals, raising the possibility that developmental duration and lifespan have some genetic or mechanistic control in common. The role of duration of development in mediating between the mechanistic levels of construction of retinal and cortical organization, and the different life histories associated with larger brains, such as duration of parental care, learning and overall longevity are discussed.