Neural progenitors, patterning and ecology in neocortical origins

Abstract

The anatomical organization of the mammalian neocortex stands out among vertebrates for its laminar and columnar arrangement, featuring vertically oriented, excitatory pyramidal neurons. The evolutionary origin of this structure is discussed here in relation to the brain organization of other amniotes, i.e., the sauropsids (reptiles and birds). Specifically, we address the developmental modifications that had to take place to generate the neocortex, and to what extent these modifications were shared by other amniote lineages or can be considered unique to mammals. In this article, we propose a hypothesis that combines the control of proliferation in neural progenitor pools with the specification of regional morphogenetic gradients, yielding different anatomical results by virtue of the differential modulation of these processes in each lineage. Thus, there is a highly conserved genetic and developmental battery that becomes modulated in different directions according to specific selective pressures. In the case of early mammals, ecological conditions like nocturnal habits and reproductive strategies are considered to have played a key role in the selection of the particular brain patterning mechanisms that led to the origin of the neocortex.

Postmitotic control of sensory area specification during neocortical development

“…T he mammalian cerebral cortex is tangentially divided into numerous distinct cytoarchitectural domains, called areas, each specialized to process specific motor, sensory or multimodal inputs from cognate thalamic nuclei [1][2][3] . Each area is radially subdivided into six neuronal layers (laminae) characterized by specific cell types, morphologies and connectivity.…”

Morphological evolution of the vertebrate forebrain: From mechanical to cellular processes

“…Likewise, the reelin-producing Cajal-Retzius cells that regulate neocortical radial migration arise in the medial and lateral pallium and migrate into the dorsal pallium and other regions (de Frutos et al, 2016;Montiel & Aboitiz, 2015;Pedraza, Hoerder-Suabedissen, Albert-Maestro, Molnár, & De Carlos, 2014;Zimmer et al, 2010). Furthermore, a transient cell population migrates from the ventral pallium into the developing neocortex in mammals and disappears around birth, but contributes to the maturation of the superficial layers in the cortical plate and possibly guides incoming mesencephalic sensory afferents to the neocortex (Aboitiz & Zamorano, 2013;Teissier et al, 2010).…”

Genetic manipulation of reptilian embryos: toward an understanding of cortical development and evolution

“…Because reptiles occupy a unique evolutionary position within amniotes, developmental analyses of the reptilian cortex illuminate commonalities and divergence of developmental programs, thus providing significant insights into the origin of the mammalian cerebral cortex. Previous studies identified unique features of reptilian corticogenesis, such as an outside-in pattern of neuronal migration (Goffinet et al, 1986 , 1999 ; Tissir et al, 2003 ; Aboitiz and Zamorano, 2013 ), a difference of layer-specific cell types produced in the reptilian dorsal pallium (Reiner, 1991 , 1993 ), a difference regarding the existence of intermediate progenitors (Charvet et al, 2009 ; Medina and Abellan, 2009 ), and lower rates of neurogenesis compared to mouse and other mammalian species (Nomura et al, 2013a ). However, modern experimental techniques have not been applied to the analyses of reptilian corticogenesis, largely because of several technical difficulties in collection and manipulation of embryos.…”