Neurogenesis in reptilian cortical structures: ³H‐thymidine autoradiographic analysis

Abstract

Histogenesis was studied in forebrain cortical areas of two reptiles, Emys orbicularis and Lacerta trilineata, by using tritiated thymidine autoradiography. Four areas were considered: the dorsomedial, the general (dorsal), and the lateral cortices, and the dorsal ventricular ridge (DVR). The bulk of neurogenesis in these four pallial fields proceeds within a short period of 8-9 days, between developmental stages 15 and 18 in Emys and stages 32-34 in Lacerta. Lateral-to-medial as well as anterior-to-posterior tangential gradients of histogenesis are present in both species. Radial neurogenetic gradients are directed from outside to inside, except in the medial cortex of lizards, where no radial gradient is seen. This pattern of histogenesis in the cortex of turtles and lizards is comparable to that in mammals in terms of timing and tangential, areal variations. It might represent a "common denominator" of cortical histogenesis. However, in contrast to the mammalian cortex, which develops according to an inside to outside, "inverted" pattern, radial neurogenesis in the cortex of turtles and lizards follows an outside-to-inside gradient. These observations suggest that the inside-out gradient of cortical neurogenesis has been acquired during evolution of the synapsid radiation from stem reptiles to mammals, and that it may be related to the development of radial cortical architectonics.

Cell Migration and Aggregation in the Developing Telencephalon: Pulse-Labeling Chick Embryos with Bromodeoxyuridine

“…Tsai et al (1981a) similarly concluded from their autoradiographic data that most of the cells born on days 6 -7 are neurons and that most of the glia are born after day 10 of embryogenesis (Goffinet et al, 1986). This is consistent with our unpublished observation that the small and irregularly shaped nuclei typically found in glia are more frequently labeled when BrdU is injected after 8 d of incubation.…”

“…From this perspective, the present data are important because they show that migration past older cells is not unique to mammalian neocortex. To determine whether the ability to migrate past older cells evolved twice independently in birds and mammals or just once, in a common ancestors of reptiles, birds, and mammals, it will be necessary to perform more detailed analyses of neurogenesis in amphibians and reptiles (Goffinet et al, 1986). Similarly, the present data show that a subpallial SVZ is not unique to mammals but, again, they leave open the question as to whether the SVZ evolved twice independently in birds and mammals or just once in a common ancestor of these two taxa.…”

“…1), whereas the mammalian neocortex develops in an inside-out manner (Angevine and Sidman, 1961;Berry and Rogers, 1965;Shimada and Langman, 1970;Rakic, 1974;Bayer et al, 1991). In fact, an inside-out pattern of neurogenesis has not been reported previously in any nonmammalian vertebrate (Goffinet et al, 1986). This suggests that one "key event" in the evolution of mammalian neocortex was the acquisition of the ability of young neocortical neurons to migrate past older cells and thus establish an inside-out pattern of neurogenesis (Butler, 1994).…”

Conserved pattern of tangential neuronal migration during forebrain development

“…Although the dorsal cortex of sauropsids (birds and reptiles) only contains a fraction of the cell types found in the mammalian isocortex (Reiner, 1991;Reiner, 1993), the two antagonistic functional classes of neurons -GABAergic and glutamatergic -are present, suggesting that they were already present in the common ancestor (Goffinet, 1983;Goffinet et al, 1986;Blanton et al, 1987;Blanton and Kriegstein, 1991a;Blanton and Kriegstein, 1991b;Reiner, 1991). The percentage and distribution of inhibitory GABAergic neurons in avian and reptilian pallial regions resemble those seen in mammals (Veenman and Reiner, 1994;Jarvis et al, 2005).…”

“…Adult turtle cortex contains the same two broad functional categories of neurons as the cortex of mammals: excitatory pyramidal and inhibitory stellate neurons (Connors and Kriegstein, 1986). Glutamatergic neurons migrate radially within the pallium and occupy their position in the cortex according to an 'outside-first to inside-last' neurogenetic gradient (Goffinet, 1983;Goffinet et al, 1986). In turtle dorsal cortex, GABAergic neurons represent only 6% of all neurons (Blanton et al, 1987), compared with a 10-20% representation in rodents and primates (Parnavelas, 2000;Hendry et al, 1987).…”