Concentric ring topology of mammalian cortical sectors and relevance for patterning studies

Abstract

Models aiming to explain causally the evolutionary or ontogenetic emergence of the pallial isocortex and its regional/areal heterogeneity in mammals use simple or complex assumptions about the pallial structure present in basal mammals and nonmammals. The question arises: how complex is the pattern that needs to be accounted for in causal models? This topic is also paramount for comparative purposes, since some topological relationships may be explained as being ancestral, rather than newly emerged. The mouse pallium is apt to be reexamined in this context, due to the breadth of available molecular markers and correlative experimental patterning results. We center the present essay on a recapitulative glance at the classic theory of concentric mammalian allo‐, meso‐, and neocortex domains. In its simplest terms, this theory postulates a central neocortical island (6 layers) separated by a surrounding mesocortical ring (4–5 layers) from a peripheral allocortical ring (3 layers). These territories show additional partition into regional or areal subdivisions. There are also borderline amygdalar, claustral, and septal areas of the pallium, nuclear in structure. There has been little effort so far to contemplate the full concentric ring model in current “cortex patterning” models. In this essay, we recapitulate the ring idea in mammals (mouse) and consider a potential causal patterning scenario using topologic models. Finally, we briefly explore how far this theory may apply to pallium models proposed recently for sauropsids.

A radial histogenetic model of the mouse pallial amygdala

“…The developmental origin of REP is still unclear and unexplored. However, the REP is clearly distinct molecularly from the EPD (i.e., is probably not lateropallial sensu Puelles 2014); notably, it does not express the characteristic lateropallial claustral Nr4a2 marker (Puelles 2014), and it also differs molecularly from the EPV, a Dbx1-LacZ-positive ventropallial derivative which is indistinctive in our AZIN2-LacZ material ( Fig. 6; Puelles et al 2016a, b).…”

In search of common developmental and evolutionary origin of the claustrum and subplate

“…In later‐stage embryos of carnivores and primates the claustrum separates cytoarchitectonically from the insular cortex primordium with the development of the extreme capsule. However, in rodents, bats, and other cases the claustrum remains embedded within the insula, though its cells keep their molecular distinctions from insular neuronal populations (Narkiewicz & Mamos, 1990; Puelles, 2014; Puelles, Alonso, García‐Calero, & Martínez‐de‐la‐Torre, 2019).…”

Histogenetic Radial Models as Aids to Understanding Complex Brain Structures: The Amygdalar Radial Model as a Recent Example

“…The first steps of neighbor-independent radial unit histogenetic activity are the processes of proliferation (surface and thickness growth), neurogenesis , and vascularization (see in this last regard Puelles et al, 2019 ). Heterochronic patterns of proliferation and neurogenesis are specified locally within the unitary neuroepithelial areas in ways still hardly investigated (Puelles et al, 1987 ).…”

“…Also, AHi was described as a derivative of the medial pallium in Abellán et al ( 2014 ). In contrast to these concepts, Puelles et al ( 2019 ) proposed recently an updated cortical ring model , which questioned a necessary one-to-one causal relationship of amygdalar pallial parts with cortical pallial subdivisions. They suggested instead that the pallial amygdala should be considered an independent non-cortical complex structure (consisting of several FMUs) located external to the cortical pallium field, irrespective of sharing some gene markers with it.…”