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. K E Y W O R D S bats, cerebral cortex, mammal, naked mole rat, retina ORCID Barbara L. Finlay http://orcid.org/0000-0003-3188-1296 Kexin Huang

Developmental Differences in Neocortex Neurogenesis and Maturation Between the Altricial Dwarf Rabbit and Precocial Guinea Pig

“…Moreover, we show that the period of cortical neurogenesis takes longer in absolute gestational days in the precocial guinea pig compared with that of the altricial dwarf rabbit. Thus, our findings are in line with previous studies suggesting precocial mammals exhibit a delayed onset and protracted duration of cortical neurogenesis when compared with phylogenetically closely related altricial mammals (Brunjes et al, 1989;Brunjes, 1990;Workman et al, 2013;Finlay and Huang, 2020). In this regard, it is interesting to note that other neurodevelopmental processes, including the transformation of the neural plate into the neural tube as well as hippocampal neurogenesis, the generation of olfactory mitral cells, and that of retinal rods and cones seem to start at a later time point after conception and to last for a longer absolute duration in the precocial guinea pig when compared with the altricial rabbit (DeSesso, 1996;Schnorr and Kressin, 2006;Workman et al, 2013).…”

“…Intriguingly, our data show that, in absolute postconceptional days, the onset of cortical neurogenesis is shifted between the two species analyzed, starting ∼10 days later in the precocial guinea pig than in the altricial dwarf rabbit. This time shift corresponds to the translating time between equivalent post conception dates of rabbit and guinea pig (Workman et al, 2013;Finlay and Huang, 2020). Moreover, we show that the period of cortical neurogenesis takes longer in absolute gestational days in the precocial guinea pig compared with that of the altricial dwarf rabbit.…”

Historical and philosophical perspectives on the study of developmental bias

“…In a similar vein, the contributions to this special issue illustrate that the study of developmental bias spans different biological domains (and thus implicates different fields): gene regulation (e.g., Hu et al, ), parthenogenesis (Galis & van Alphen, ), phenotypic plasticity (Draghi, ; Levis & Pfennig, ; Parsons et al, ; Uller et al, ), the morphology of extant and fossil species (Jablonski, ; Jackson, ), brain development (Finlay & Huang, ), symbiosis and interactions involving microbial species (Gilbert, ), development of the vertebrate skeleton (Kavanagh, ), and behavior, learning, and niche construction (Hu et al, ; Laland et al, ), among others. Some of the studies are experimental, some include field work, and others make primarily use of theory and computational simulation (Draghi, ; Hordijk & Altenberg, ).…”

Cutting across structural and transcriptomic scales translates time across the lifespan in humans and chimpanzees

“…These studies highlight the role of protracted development in establishing connections and maturation of projections supporting neural structures unique to humans. The developmental time course of connection formation and projection maturation may be the product of an extended duration of development in humans relative to other species [21][22][23][24][25]. It is therefore not clear whether connection formation and projection maturation are extended in humans relative to chimpanzees once variation in developmental schedules is controlled for across species.…”