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Review
. 2021 Feb 15:9:591017.
doi: 10.3389/fcell.2021.591017. eCollection 2021.

Genetic Mechanisms Underlying Cortical Evolution in Mammals

Lucía Florencia Franchini  1
Affiliations
Review

Genetic Mechanisms Underlying Cortical Evolution in Mammals

Lucía Florencia Franchini. Front Cell Dev Biol. .

Abstract

The remarkable sensory, motor, and cognitive abilities of mammals mainly depend on the neocortex. Thus, the emergence of the six-layered neocortex in reptilian ancestors of mammals constitutes a fundamental evolutionary landmark. The mammalian cortex is a columnar epithelium of densely packed cells organized in layers where neurons are generated mainly in the subventricular zone in successive waves throughout development. Newborn cells move away from their site of neurogenesis through radial or tangential migration to reach their specific destination closer to the pial surface of the same or different cortical area. Interestingly, the genetic programs underlying neocortical development diversified in different mammalian lineages. In this work, I will review several recent studies that characterized how distinct transcriptional programs relate to the development and functional organization of the neocortex across diverse mammalian lineages. In some primates such as the anthropoids, the neocortex became extremely large, especially in humans where it comprises around 80% of the brain. It has been hypothesized that the massive expansion of the cortical surface and elaboration of its connections in the human lineage, has enabled our unique cognitive capacities including abstract thinking, long-term planning, verbal language and elaborated tool making capabilities. I will also analyze the lineage-specific genetic changes that could have led to the modification of key neurodevelopmental events, including regulation of cell number, neuronal migration, and differentiation into specific phenotypes, in order to shed light on the evolutionary mechanisms underlying the diversity of mammalian brains including the human brain.

Keywords: brain; cetacea; cortex; elephant; human; human accelerated region; primates; synapsids.

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Conflict of interest statement

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Phylogenetic tree of mammalian evolution. The schematic phylogenetic tree has been based on phylogenetic trees built by Goffinet (2017) and Rowe (2017). Red lines mark the mass extinction events. In every lineage two examples of lissencephalic and gyrencephalic brains are shown. Extinct lineages show examples of species that have been described from fossils specimens. Drawings of Therapsid Proburnetia viatkensis Tatarinov species and Cynodont Kayentatherium wellesi Kermack species were performed by the artist Nobu Tamura (http://spinops.blogspot.com/) and reproduced with permission.
Figure 2
Figure 2
Cortex across amniota. (A) Schematics of coronal sections at the forebrain in amniotes. On the left a drawing of the developing mammalian forebrain (based on the mouse) indicating the location of the neocortex (NCx), medial cortex (MC), lateral cortex (LC), and ventral telencephalic structures such as the lateral and medial ganglionic eminences (LGE and MGE). In the middle and at the right schematics of the reptile and bird forebrains showing dorsal cortex (DC), medial cortex, lateral cortex, hyperpallium or Wulst (W), and subpallial structures as the dorsal ventricular ridge (DVR). The approximate location of the striatum is also indicated (ST). Colors indicate brain regions that are homologous among the different vertebrate lineages. Rectangles in mammal and reptile brains indicate approximate location of the layers schematic shown in (C). (B) A Nissl stained coronal section of the adult macaca rhesus forebrain is shown. The rectangle indicates the approximate location of the magnification shown at the right. Magnification shows layers of the neocortex. (C) Schematic of the six layers of the neocortex in the adult mammalian neocortex. Next, a drawing shows the three layers of the dorsal cortex in a reptile. (D) Representational drawings of the developing neocortex of a gyrencephalic primate and a lissencephalic rodent where the germinative zones and cellular types are indicated. Next to it, the different cellular types of the adult and the embryonic developing neocortex are indicated. Macaque rhesus (Macaca mulatta) brain slices are from BrainMaps: An Interactive Multiresolution Brain Atlas; http://brainmaps.org.
Figure 3
Figure 3
Phylogenetic tree of primates and related mammalian orders. On the top row representative brains of the different groups that composed the Euarchontoglires clade are shown. Primate groups and approximate times of divergence are indicated on the tree. The arrows indicated moments in history where brain volume has increased in the Anthropoid lineage according to Goodman (1999). Brain pictures are approximately at scale and are from the Comparative Mammalian Brain Collection (http://neurosciencelibrary.org) from the University of Wisconsin and Michigan State Comparative Mammalian Brain Collections, as well as from those at the National Museum of Health and Medicine funded by the National Science Foundation, as well as by the National Institutes of Health.
Figure 4
Figure 4
Prefrontal cortex in primates. Pictures of representative primate groups and the rat show the approximate location of the lateral Prefrontal Cortex (lPFC). Brain pictures are approximately at scale and are from the Comparative Mammalian Brain Collection (http://neurosciencelibrary.org) from the from the University of Wisconsin and Michigan State Comparative Mammalian Brain Collections, as well as from those at the National Museum of Health and Medicine funded by the National Science Foundation, as well as by the National Institutes of Health.
Figure 5
Figure 5
Genetic changes underlying human nervous system evolution. A schematic phylogenetic tree shows the relationships among macaque, chimpanzee and human. Above that brain pictures show a detail of the size differences among these three primate species. Brains are shown at scale. On top of that, brain coronal sections at the forebrain level show anatomic differences among the species. It is appreciated the great development of the gyrification in the three species. Brain pictures are approximately at scale and are from the Comparative Mammalian Brain Collection (http://neurosciencelibrary.org) from the from the University of Wisconsin and Michigan State Comparative Mammalian Brain Collections, as well as from those at the National Museum of Health and Medicine funded by the National Science Foundation, as well as by the National Institutes of Health. On the lineage leading to humans some salient genetic changes that have been uncovered in the last years are indicated. PE, positively selected genes; DG, duplicated genes.
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