Homology, neocortex, and the evolution of developmental mechanisms

Abstract

The six-layered neocortex of the mammalian pallium has no clear homolog in birds or non-avian reptiles. Recent research indicates that although these extant amniotes possess a variety of divergent and nonhomologous pallial structures, they share a conserved set of neuronal cell types and circuitries. These findings suggest a principle of brain evolution: that natural selection preferentially preserves the integrity of information-processing pathways, whereas other levels of biological organization, such as the three-dimensional architectures of neuronal assemblies, are less constrained. We review the similarities of pallial neuronal cell types in amniotes, delineate candidate gene regulatory networks for their cellular identities, and propose a model of developmental evolution for the divergence of amniote pallial structures.

Figure 1

The amniotes and their pallial anatomies Amniotes include mammals and sauropsids (birds and non-avian reptiles). Tuataras, together with snakes and lizards (not shown), form the lepidosaurs. A second major group of sauropsids, the archosaurs, includes birds and crocodilians. Schematic tracings of telencephalon anatomies are shown as left-side coronal cross sections with medial to the right and dorsal at the top. All amniotes have a ventral telencephalon (VT, grey shading) and a dorsal telencephalon, or pallium (yellow shading). The mammalian pallium includes the neocortex (Ncx), piriform cortex (CPi), hippocampus (not shown), and amygdala (not shown). The pallium in non-avian reptiles includes a dorsal ventricular ridge (DVR) and a cerebral cortex with medial (MC), dorsal (DC), and lateral (LC) divisions. The bird DVR contains the ventral part of the mesopallium (M), the nidopallium (N), the entopallium (E), and the arcopallium (not shown). Birds have a medial hippocampus (Hp), a lateral piriform cortex (CPi), and a dorsally located Wulst that includes the dorsal mesopallium and the hyperpallium (H). Figure adapted from (18). Drawings are not to scale.

Figure 2

Evolution of excitatory neocortical cell types and circuitry The common ancestor of amniotes is hypothesized to have had input (green), output (red), and intratelencephalic (IT, blue) pallial neurons. Input neurons receive primary sensory information from the dorsal thalamus (dTh), whereas output neurons extend axons from the pallium to the brainstem (Bst). IT neurons serve as a relay between input and output neurons, and additionally project to the striatum. These three principal pallial cell types were reorganized into the divergent architectures of the neocortex, dorsal cortex, Wulst, and the DVR (not shown). Candidate transcriptional regulators of cell identity are depicted within the ancestral cell types (, –18). The evolutionary origin of neocortical corticothalamic neurons (black cells in L6) is not known (18). The pallial inhibitory interneurons, derived from the ventral telencephalon, are not indicated (but see (16)). Figure adapted from (18). HA, hyperpallium apicale; IHA, interstitial nucleus of the hyperpallium apicale; L, layer; Md, dorsal mesopallium.

Figure 3

Anatomical transformations during the evolutionary diversification of amniote pallial structures The hypothetical amniote last common ancestor had an architecturally simple pallium, which contained input (green), output (red), IT (blue), and hippocampal (orange) cell types. The ancestral pallium underwent independent evolutionary transformations to give rise to the mammalian neocortex and the sauropsid DVR, dorsal cortex, and Wulst. The pink arrows note an expansion of the lateral pallium with the origin of the DVR in early sauropsids. This expansion may have accompanied the origin of non-input nidopallium cells (pink). DVR input nuclei are embedded within the nidopallium. v, ventricle; VT, ventral telencephalon.

Figure 4

Pallium evolution resembles an hourglass A field of embryonic neuronal progenitors (grey cells, bottom center) can be developmentally patterned such that pallial cell types arise from all parts of the neuroepithelium, as in mammals (bottom left), or from restricted parts of the neuroepithelium as in sauropsids (bottom right). Pallial cell types are specified to form conserved connections (middle of hourglass), possibly through conserved transcriptional regulators (see Figure 2), but migrate to form clade-specific cortical or nuclear architectures (top).