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Figure 1 Summary of geological epochs, and simplified evolutionary filiations of amniotes. Numbers refer to estimated time of phyletic divergence (in mega-years (Myrs)). Adapted from Bar, I., Lambert de Rouvroit, C., and Goffinet, A. M. 2000. The evolution of cortical development. An hypothesis based on the role of the reelin signaling pathway. Trends Neurosci. 23, 633-638, with permission from Elsevier.

Figure 1 Summary of geological epochs, and simplified evolutionary filiations of amniotes. Numbers refer to estimated time of phyletic divergence (in mega-years (Myrs)). Adapted from Bar, I., Lambert de Rouvroit, C., and Goffinet, A. M. 2000. The evolution of cortical development. An hypothesis based on the role of the reelin signaling pathway. Trends Neurosci. 23, 633-638, with permission from Elsevier.

amniotes, telencephalic development follows a basic, evolutionary homologous Bauplan. This basic organization includes a medial, dorsal, and lateral cortex located at the external aspect of the ventricle, and the dorsal ventricular ridge (DVR) located ventral to the ventricle (Figure 2). There is a consensus that the medial cortex is homologous to the mammalian hip-pocampal formation, whereas the dorsal and lateral cortices are the precursors of the neocortex and the pyriform cortex or rhinencephalon, respectively. Views about the DVR, which is diminutive in mammals, are more controversial (Northcutt, 1981; Butler and Hodos, 1996; Fernandez et al., 1998).

In mammals, cortical development begins with the appearance of the PP (Caviness, 1982; Allendoerfer and Shatz, 1994; Sheppard and Pearlman, 1997; Super et al., 2000), a heterogeneous structure that contains future subplate cells, reelin-negative pioneer neurons and reelin-positive subpial cells destined for the MZ (Meyer et al., 1998,2000), and probably other cell types. The next stage is the condensation of the CP, densely populated with radial bipolar neurons. The appearance of the CP results in the splitting of the PP, elements of which are displaced in the subplate (Allendoerfer and Shatz, 1994) and in the MZ (Caviness, 1982; Sheppard and Pearlman, 1997). The CP develops from inside to outside, by migration of new neurons that cross previously established layers and settle at progressively more superficial levels. The organization of the CP is controlled by the reelin-sig-naling pathway (Rice and Curran, 2001; Tissir and Goffinet, 2003). Defective reelin signaling results in a loosely organized CP, with absence of PP splitting, and inverted maturation, from outside to inside (Caviness and Rakic, 1978; Rakic and Caviness, 1995). Normal reelin signaling is necessary but not sufficient for the development of the CP. For example, in mice deficient in cyclin-dependent kinase 5 (Cdk5) or its cofactors p35 and p39 (Ohshima et al., 1996; Chae et al., 1997; Gilmore et al., 1998; Ko et al., 2001), the radial organization of the early CP is preserved, yet its maturation proceeds from outside to inside as in

Embryonic Cortex Striatum

Figure 2 Schematic organization (frontal sections) of the dorsal embryonic telencephalon in putative stem amniotes, chelonians (turtles), squamates (lizards and snakes), archosaurs (birds and crocodiles), and mammals. BF, basal forebrain; DC, dorsal cortex (mammalian NC, neocortex); DVR, dorsal ventricular ridge; LC, lateral cortex (mammalian Rh, rhinencephalon); MC, medial cortex (mammalian Hip, hippocampus); MGEand LGE, medial and lateral ganglionic eminences; Sep, septal nuclei; Str, striatum; Wu, avian Wulst. Reproduced from Bar, I., Lambert de Rouvroit, C., and Goffinet, A. M. 2000. The evolution of cortical development. An hypothesis based on the role of the reelin signaling pathway. Trends Neurosci. 23, 633-638, with permission from Elsevier.

Figure 2 Schematic organization (frontal sections) of the dorsal embryonic telencephalon in putative stem amniotes, chelonians (turtles), squamates (lizards and snakes), archosaurs (birds and crocodiles), and mammals. BF, basal forebrain; DC, dorsal cortex (mammalian NC, neocortex); DVR, dorsal ventricular ridge; LC, lateral cortex (mammalian Rh, rhinencephalon); MC, medial cortex (mammalian Hip, hippocampus); MGEand LGE, medial and lateral ganglionic eminences; Sep, septal nuclei; Str, striatum; Wu, avian Wulst. Reproduced from Bar, I., Lambert de Rouvroit, C., and Goffinet, A. M. 2000. The evolution of cortical development. An hypothesis based on the role of the reelin signaling pathway. Trends Neurosci. 23, 633-638, with permission from Elsevier.

reelin-deficient mice. Two reelin-dependent developmental events, CP organization and inside-out maturation, were presumably also important acquisitions during cortical evolution (Bar et al., 2000). Additional factors of cortical evolution include increased neuron generation in the ventricular zone (VZ) and the necessity to migrate over longer distances, requiring a sophisticated migration machinery in which Cdk5, p35/p39, and other genes such as filamin-1, Lisi, or doublecortin participate (Lambert de Rouvroit and Goffinet, 2001; Grove and Fukuchi-Shimogoril, 2003).

Reelin is a large extracellular glycoprotein that is secreted by Cajal-Retzius neurons in the MZ (Bar et al., 1995; D'Arcangelo et al., 1995). It binds to two receptors of the lipoprotein receptor family, very low density lipoprotein receptor (VLDR) and apolipoprotein E receptor type 2 (ApoER2) that are expressed at the surface of CP cells (Hiesberger et al., 1999; Trommsdorff et al., 1999). This triggers the activation of an intracellular signal that ultimately directs the architectonic organization of the CP. Upon reelin-receptor binding, the adapter disabled-1 gene or protein (Dab1) is tyrosine phosphorylated by

Scr family kinases (Howell et al., 200( ), but the rest of the mechanism is still poorly understood (Bock et al., 2003; Pramatarova et al., 2003; Ballif et al., 2004; Jossin et al., 2004).

Reelin and Dabl expression have been studied in mouse (Rice and Curran, 2001; Tissir and Goffinet, 2003), human (Meyer and Goffinet, 1998; Meyer et al., 2002, 2003), turtle (Bernier et al., 1999), lizard (Goffinet et al., 1999), chick (Bernier et al., 2000), and crocodile (Tissir et al., 2003), allowing comparisons and correlations with architectonic patterns in representatives of the main amniote lineages (Figure 3; Goffinet, 1983). The expression of VLDLR and ApoER2 is supposed to overlap largely that of Dab1, but this remains to be studied. In turtles, which are considered the most closely related to stem amniotes, cortical architectonics is the most rudimentary. Reelin-positive neurons are present in the MZ of the medial and dorsal cortical fields. In addition, some less strongly labeled neurons are dispersed in the CP. The situation in the lateral cortex is different, with reelin-positive neurons scattered diffusely in the cortex (Bernier et al., 1999). Dab1 is expressed in CP cells in all sectors

Sagittal Lung

Figure 3 Comparison of reelin mRNA expression. Frontal sections in the embryonic cortex of the mouse (a, a'), turtle (b, b'), lizard (c, c') and chick (d, d'). Expression patterns of reelin mRNA are shown in darkfield views (a-d). Schematic drawings (a'-d') show reelin-positive zones (circles for cells in marginal zone, and hatched areas for more diffuse expression in cortical plate or subcortex). CP, cortical plate; DC, dorsal cortex; DVR, dorsal ventricular ridge; LC, lateral cortex; MC, medial cortex; V, ventricle.

a, a', The mouse cortex is characterized by an almost continuous subpial layer of neurons that express extremely high levels of reelin. The underlying CP is reelin-negative but expresses Dab1. Detailed descriptions are provided in Alcantara et al. (1998) and Schiffmann et al. (1997).

b, b', In the turtle cortex, reelin-positive cells (arrows) are dispersed in the marginal zones of the MCand DC, and to a lesser extent in the lateral cortex and DVR. The cortical plate in MC and DC is weakly reelin-positive and Dabl-positive. Arrowheads point to spontaneously darkfield-positive melanophores. Detailed description in Bernier et al. (1999).

c, c', In the lizard MC and DC, reelin-positive neurons (arrows) are abundant in the marginal zone, and there is a second layer of reelin expression in the subplate (hatched area in c'), whereas the cortical plate is reelin-negative but Dab1-positive. The LC is diffusely Dab1-positive, and its dorsal component expresses reelin (hatched in c'). Detailed description in Goffinet etal. (1999).

d, d', In the chick, subpial reelin-positive cells (arrows) are found only in the diminutive MC (hippocampus) and DC (parahippo-campus), and the cortical plate is negative. There is diffuse reelin expression in the LC. Detailed description in Bernier et al. (2000).

Figure 3 Comparison of reelin mRNA expression. Frontal sections in the embryonic cortex of the mouse (a, a'), turtle (b, b'), lizard (c, c') and chick (d, d'). Expression patterns of reelin mRNA are shown in darkfield views (a-d). Schematic drawings (a'-d') show reelin-positive zones (circles for cells in marginal zone, and hatched areas for more diffuse expression in cortical plate or subcortex). CP, cortical plate; DC, dorsal cortex; DVR, dorsal ventricular ridge; LC, lateral cortex; MC, medial cortex; V, ventricle.

a, a', The mouse cortex is characterized by an almost continuous subpial layer of neurons that express extremely high levels of reelin. The underlying CP is reelin-negative but expresses Dab1. Detailed descriptions are provided in Alcantara et al. (1998) and Schiffmann et al. (1997).

b, b', In the turtle cortex, reelin-positive cells (arrows) are dispersed in the marginal zones of the MCand DC, and to a lesser extent in the lateral cortex and DVR. The cortical plate in MC and DC is weakly reelin-positive and Dabl-positive. Arrowheads point to spontaneously darkfield-positive melanophores. Detailed description in Bernier et al. (1999).

c, c', In the lizard MC and DC, reelin-positive neurons (arrows) are abundant in the marginal zone, and there is a second layer of reelin expression in the subplate (hatched area in c'), whereas the cortical plate is reelin-negative but Dab1-positive. The LC is diffusely Dab1-positive, and its dorsal component expresses reelin (hatched in c'). Detailed description in Goffinet etal. (1999).

d, d', In the chick, subpial reelin-positive cells (arrows) are found only in the diminutive MC (hippocampus) and DC (parahippo-campus), and the cortical plate is negative. There is diffuse reelin expression in the LC. Detailed description in Bernier et al. (2000).

(Goffinet, unpublished). In chicks (Bernier et al., 2000), a CP is evident only in the medial cortex and in the adjacent, dorsal parahippocampal cortex. At this level, a few strongly reelin-positive neurons are found in the MZ, but not in the CP itself. A similar canvas of reelin-positive cells in the MZ and reelin-negative CP is found in crocodiles (Tissir et al., 2003). Dabl expression has not been studied in the chick and crocodilian telencephalon.

In lizards (squamates), an elaborate architectonic organization of the medial and dorsal cortices develops in parallel with a specific, bilaminar expression of reelin, bracketing a reelin-negative and Dabl-positive CP (Goffinet et al., 1999). Large reelin-positive neurons are present in the MZ, as in other species. Unlike in other amniotes, a second layer of reelin-positive cells is found in the subcortex. As in turtles, the lateral cortex expresses both reelin and

Dabi. In turtles, lizards, and chicks, maturation of the CP proceeds from outside to inside (as in reelin-deficient mammals; Tsai et al., 1981; Goffinet et al., 1986). Mammals (synapsids) are characterized by a spectacular development of the CP both in terms of cell numbers and architectonic organization, and by its maturation from inside to outside (Caviness and Rakic, 1978; Rakic and Caviness, 1995). This is accompanied by an amplification of reelin production in Cajal-Retzius cells (CRc) - as estimated using in situ hybridization with species-specific probes and monoclonal antibodies with conserved epitopes - and anomalies in reelin-deficient mice indicate that this modification of reelin expression was necessary for the evolution of the mammalian cortex.

Although several pieces of the puzzle are lacking, such as the expression of lipoprotein receptors and the analysis of more species, these data clearly suggest that the production of reelin by early neurons in the MZ and the expression of Dab1 (and reelin receptors) by CP neurons is a feature of all amniotes. This pattern, presumably present in stem amniotes, is evolutionarily homologous. From this ancestral pattern, the expression profiles have evolved differently in divergent lineages; similar elaborate CP organizations in mammals and in some cortical areas in lizards were probably acquired by convergent evolution. In addition to the control of neuronal numbers and differentiation, and of hodological relationships, the modulation of architectonic organization is an important, hitherto neglected, parameter of cortical evolution, in which the reelin-signaling pathway plays an important role.

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