Molecular and cellular evolution of corticogenesis in amniotes

Abstract

The cerebral cortex varies dramatically in size and complexity between amniotes due to differences in neuron number and composition. These differences emerge during embryonic development as a result of variations in neurogenesis, which are thought to recapitulate modifications occurred during evolution that culminated in the human neocortex. Here, we review work from the last few decades leading to our current understanding of the evolution of neurogenesis and size of the cerebral cortex. Focused on specific examples across vertebrate and amniote phylogeny, we discuss developmental mechanisms regulating the emergence, lineage, complexification and fate of cortical germinal layers and progenitor cell types. At the cellular level, we discuss the fundamental impact of basal progenitor cells and the advent of indirect neurogenesis on the increased number and diversity of cortical neurons and layers in mammals, and on cortex folding. Finally, we discuss recent work that unveils genetic and molecular mechanisms underlying this progressive expansion and increased complexity of the amniote cerebral cortex during evolution, with a particular focus on those leading to human-specific features. Whereas new genes important in human brain development emerged the recent hominid lineage, regulation of the patterns and levels of activity of highly conserved signaling pathways are beginning to emerge as mechanisms of central importance in the evolutionary increase in cortical size and complexity across amniotes.

Keywords: Chick; Mouse; Neurogenesis; Primate; Radial Glia; Robo.

Fig. 1

Vertebrate phylogeny. Simplified phylogenetic tree of vertebrates, illustrating the appearance of representative species and their brains. Drawings are not at scale

Fig. 2

Schematic drawings of coronal sections through the telencephalon of amniotes indicating the extent of subdivisions. a Early embryonic telencephalon of a model amniote. b–d Adult telencephalon of reptiles, birds and mammals, as indicated, based on the tetrapartite model [25]. The subpallium is represented in gray and subdivisions of the pallium are color coded as indicated. The striped pattern in the reptile and bird pallium indicates the extension of the DVR. Hp hippocampus, DCx dorsal cortex, Cl claustrum, Ins insula, EPn endopiriform nucleus, PC piriform cortex, Amygd amygdala, DVR dorsal ventricular ridge, Hyp hyperpallium, NCx neocortex

Fig. 3

Brain size and modes of neurogenesis in the pallium of vertebrates. a Simplified phylogenetic tree of vertebrates with schematic drawings at scale of the brain of model species in cross section. Differences in brain size between model species are proportional to their relative encephalization quotient (brain-to-body mass ratio) [29, 236]. Red and gray areas correspond to the pallium and subpallium, respectively. For monotremes, marsupials and primates, only a portion of the telencephalon can be shown at scale due to differences in size. Black dashed boxes indicate the brain areas shown in the drawings at scale. b Schematic drawings of germinal layers and types of progenitor cells in the embryonic pallium of vertebrates. Background colors group the clades according to their germinal layers: green, only ventricular zone (VZ); blue, VZ + subventricular zone (SVZ); orange, VZ + inner SVZ (iSVZ) + outer SVZ (oSVZ). The relative abundance of progenitor cell types in each group is also represented. aRGC apical radial glia cell, IPC intermediate progenitor cell, bRGC basal radial glia cell

Fig. 4

Modes of neurogenesis and neuron number in the pallium of amniotes. Schematic drawings of the adult brains of representative reptile, bird, rodent and human, and schemas of their embryonic pallium depicting the germinal layers, types of neurogenic progenitor cells and mode of neurogenesis. Reptiles only have ventricular zone (VZ) and apical radial glial cells (aRGCS, green), so all cortical neurons are produced by direct neurogenesis. Neurons (red) resemble those in deep layers of the mammalian neocortex. Birds show the first signs of a subventricular zone (SVZ), populated by intermediate progenitor cells (IPCs, blue), and an incipient shift towards indirect neurogenesis, leading to the generation of a greater amount of neurons. In mammals, IPCs and indirect neurogenesis become much more predominant, and new types of neurons are produced to establish superficial layers (violet). Neuron production is increased even further in gyrencephalic mammals like humans, by greatly expanding the SVZ into two distinct germinal layers: inner SVZ (iSVZ) and outer SVZ (oSVZ). These secondary germinal layers accumulate an exceptional abundance of basal progenitor cells: IPCs and basal radial glia cells (bRGCs, orange). Newborn neurons migrate through the intermediate zone (IZ, gray) to reach their final destination in the neuronal layer (NL) or cortical plate (CP) (red). Arrow thickness represents the relative frequency of each mode of neurogenesis