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Review
. 2013 Nov 12:7:38.
doi: 10.3389/fnana.2013.00038. eCollection 2013.

Neural progenitors, patterning and ecology in neocortical origins

Francisco Aboitiz  1 , Francisco Zamorano
Affiliations
Review

Neural progenitors, patterning and ecology in neocortical origins

Francisco Aboitiz et al. Front Neuroanat. .

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.

Keywords: Pax6; antihem; cortical hem; dorsal ventricular ridge; intermediate progenitors; nidopallium; reelin; subventricular zone.

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Figures

FIGURE 1
FIGURE 1
Neocortical development. The deep ventricular zone (VZ) and the subventricular zone (SVZ) are the compartments where cell proliferation takes place. (A) In early cortical development, primary neural progenitors or radial glia (RG) in the VZ divide and give rise to early neurons that migrate to the preplate (PP), and then make up the embryonic subplate (SPl). (B, C) Later in development, radial glia generate intermediate progenitors (IP), that keep dividing and producing neurons into the emerging cortical plate (CP, future layers VI–II of the neocortex), in an inside-out gradient where deep layers (VI–V) are formed first and mostly derive from progenitors in the VZ, and superficial layers (IV–II) are formed later, deriving from progenitors in the SVZ. The more superficial layer (Layer I) is the remnant of the embryonic marginal zone (MZ), in which Reelin-producing Cajal-Retzius neurons are located.
FIGURE 2
FIGURE 2
The cerebral hemispheres of reptiles and mammals. The pallium of reptiles has medial/dorsomedial (MC), dorsal (DC, corresponding to the avian hyperpallium) and lateral (LC) cortices; and a dorsal ventricular ridge, whose anterior part (ADVR) corresponds to the avian nido and mesopallium. The MC of reptiles corresponds to the hippocampus (HIP) of mammals, and the LC is homologous to the mammalian olfactory cortex (OC). The mammalian neocortex (NC) comprises two moieties, one dorsal (NCd, receiving lemnothalamic somatosensory and visual inputs), and one lateral (NCl, receiving auditory and visual collothalamic inputs). AM, pallial amygdalar formation, CL, claustrum, CS, corpus striatum, PSP, pallial-subpallial boundary.
FIGURE 3
FIGURE 3
Above, dorsal and ventral patterning centers in the cerebral hemispheres, and presumed ancestral condition. The dorsally located cortical hem (CH) expresses dorsalizing factors like Wnts and Emxs and patterns the embryonic medial pallium (MP, hippocampal formation and homologous structures) and the dorsal pallium (DP, neocortex in mammals; dorsal cortex/hyperpallium in sauropsids). On the other hand, the antihem, induced by Pax6 activity, specifies the ventral pallium (pallial amygdala in mammals, DVR/nidopallium in sauropsids). Pax 6 is expressed in a anteroventral-to-caudodorsal gradient that counteracts with the dorsalizing factors, and contributes also to neocortical and hippocampal patterning in mammals. In the common ancestor, perhaps similar of present-day amphibians, there was possibly a relatively large dorsal pallium, at the expense of the development of other pallial regions (Northcutt, 2013). Below, hypothetical scenario of developmental evolution in the pallium of amniotes. Pax6 is proposed here as a candidate to drive the amplification of progenitor proliferation in the brains of different amniotes, but there may be other or additional factors contributing to this process. Pax6 expression is proposed to have been upregulated in both sauropsids and mammals. In reptiles, this event produced a modest amplification of the antihem (AH) and the ventral pallium (VP), giving rise to the dorsal ventricular ridge. In birds, Pax6 amplification reached higher levels, expanding the nidopallium and mesopallium, and also reaching the DP, contributing to generate the hyperpallium. Conversely, in mammals, in addition to Pax6 enhancement there was a concomitant upregulation of dorsal signals (illustrated by an increase in Wnt and Emx activities), which antagonized Pax6 signaling, restricting the expansion of the antihem. Furthermore, in mammals, upregulation of Pax6 and dorsal signals show a significant overlap, allowing Pax6 to influence the expansion of the DP, giving rise to the neocortex. Not shown for simplicity is the anterior forebrain, patterned by the action of FGFs, which may have also contributed to brain expansion particularly in mammals. Note that the subpallium also increased in size in all amniotes. SP, subpallium, marked by the expression of markers like Dlx1/2.
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