Hypothesis on the Dual Origin of the Mammalian Subplate

Abstract

The development of the mammalian neocortex relies heavily on subplate. The proportion of this cell population varies considerably in different mammalian species. Subplate is almost undetectable in marsupials, forms a thin, but distinct layer in mouse and rat, a larger layer in carnivores and big-brained mammals as pig, and a highly developed embryonic structure in human and non-human primates. The evolutionary origin of subplate neurons is the subject of current debate. Some hypothesize that subplate represents the ancestral cortex of sauropsids, while others consider it to be an increasingly complex phylogenetic novelty of the mammalian neocortex. Here we review recent work on expression of several genes that were originally identified in rodent as highly and differentially expressed in subplate. We relate these observations to cellular morphology, birthdating, and hodology in the dorsal cortex/dorsal pallium of several amniote species. Based on this reviewed evidence we argue for a third hypothesis according to which subplate contains both ancestral and newly derived cell populations. We propose that the mammalian subplate originally derived from a phylogenetically ancient structure in the dorsal pallium of stem amniotes, but subsequently expanded with additional cell populations in the synapsid lineage to support an increasingly complex cortical plate development. Further understanding of the detailed molecular taxonomy, somatodendritic morphology, and connectivity of subplate in a comparative context should contribute to the identification of the ancestral and newly evolved populations of subplate neurons.

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

“…Subplate cells are some of the earliest generated neurons in cortex (Rakic and Kostovic, 1990; Hoerder‐Suabedissen et al, 2009; Oeschger et al, 2012; Hoerder‐Suabedissen, 2013). These studies strengthen the hypothesis that an embryonic subplate was present in the ancestors of mammals and that additional cellular populations evolved as cortical development and connectivity became more complex (Montiel et al, 2011; Wang et al, 2011a). In the human cortex we observed that subplate subpopulations show increased compartmentalization and that these segregate into sublayers (Hoerder‐Suabedissen and Molnár, 2015).…”

Postmitotic control of sensory area specification during neocortical development

“…Moreover, although cortical inactivation of COUP-TFI affects TCA topography (ref. Thus, the remarkable rescue of sensory thalamo-cortical innervation after COUP-TFI cortical overexpression might be due to the restored specification of cortical SP neurons, which extend their axons towards the dorsal thalamic nuclei favouring correct TCA positioning in the neocortex 34,[50][51][52][53] . Finally, we cannot exclude a direct control of COUP-TFI postmitotic gradient on molecular cues driving TCA pathfinding.…”

Comments on the Updated Tetrapartite Pallium Model in the Mouse and Chick, Featuring a Homologous Claustro-Insular Complex

“…Associated with this large-scale change we see an important development in mammals of the Cajal-Retzius population in layer 1 and the subplate population in layer 6b, which apparently include or are largely formed by tangentially migrated cells [see Montiel et al, 2011;Pedraza et al, 2014;Puelles, 2014;Watson and Puelles, 2017]. Moreover, the tangential subventricular migration of VPall Pierani neurons into the whole isocortical plate [Teissier et al, 2010;Puelles, 2011] exerts a mitogenic effect on mouse DPall progenitors, leading to an increase in cortical cellularity of about 25% [Teissier et al, 2012].…”