From sauropsids to mammals and back: New approaches to comparative cortical development

Abstract

Evolution of the mammalian neocortex (isocortex) has been a persisting problem in neurobiology. While recent studies have attempted to understand the evolutionary expansion of the human neocortex from rodents, similar approaches have been used to study the changes between reptiles, birds, and mammals. We review here findings from the past decades on the development, organization, and gene expression patterns in various extant species. This review aims to compare cortical cell numbers and neuronal cell types to the elaboration of progenitor populations and their proliferation in these species. Several progenitors, such as the ventricular radial glia, the subventricular intermediate progenitors, and the subventricular (outer) radial glia, have been identified but the contribution of each to cortical layers and cell types through specific lineages, their possible roles in determining brain size or cortical folding, are not yet understood. Across species, larger, more diverse progenitors relate to cortical size and cell diversity. The challenge is to relate the radial and tangential expansion of the neocortex to the changes in the proliferative compartments during mammalian evolution and with the changes in gene expression and lineages evident in various sectors of the developing brain. We also review the use of recent lineage tracing and transcriptomic approaches to revisit theories and to provide novel understanding of molecular processes involved in specification of cortical regions. J. Comp. Neurol. 524:630–645, 2016. © 2015 The Authors. The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

Origin and evolution of developmental enhancers in the mammalian neocortex

“…1A) (23). In each species, we examined three time points spanning critical events of corticogenesis, including the emergence of multiple transient proliferative embryonic zones in the dorsal pallium, which may be a mammal-specific characteristic; genesis and migration of cortical neurons; and initiation of neuronal connections (17,22,28). To infer neocortical enhancers that were likely active in the mammalian stem lineage, we identified enhancer regions in human and mouse that showed reproducible activity in both species based on epigenetic signatures (Fig.…”

“…Nonmammalian vertebrates lack the six-layered forebrain architecture that defines the mature neocortex (17,18). Adult structures derived from the dorsal pallium in birds and reptiles are vastly different from the neocortex at the structural, functional, and molecular level, complicating efforts to understand how the neocortex evolved (18)(19)(20)(21)(22). A recent study reported major transcriptomic divergence between the adult mouse neocortex and various chicken forebrain structures, supporting the hypothesis that mammal-specific regulatory functions contribute to the divergent morphology of the mammalian neocortex (20).…”

Circuits Regulating Pleasure and Happiness: The Evolution of the Amygdalar-Hippocampal-Habenular Connectivity in Vertebrates

“…sharks and rays, or ratfishes and chimeras), Osteichthyes (bony fishes divided into ray-finned fishes and the lobe-limbed vertebrates), Amphibia (amphibians represented by toads and frogs), Reptilia (reptiles: turtles, lizards, snakes) and Aves (birds) and Mammalia (mammals: opossums, mice, rats, cats) including Primates (primates: monkeys, apes, humans) correspond to the brains of our human ancestors from about 560 million years ago until the present (Moreno and González, 2011). A special position is taken by lungfish (a lobe-finned fish, closest ancestor of all tetrapods) and turtles as being comparable to ancient creatures which appear to be the most precisely positioned within this evolutionary line, while more recent reptiles and birds (sauropsids) appear to derive from another line of turtle-like ancestors rather than mammals (Butler et al, 2011; Moreno and González, 2011; Montiel et al, 2016). The very first vertebrate is considered to be an animal comparable with modern lamprey; this animal has a head containing a brain and has vertebrates, but not yet a lower jaw.…”

Circuits regulating pleasure and happiness: evolution and role in mental disorders

“…However, this expansion occurred along different lines in non-synapsid (turtles, reptiles, birds) and synapsid (mammals) animals (36,37). The dorsal thalamus consists of two divisions called lemnothalamus and collothalamus.…”