Quail-chick grafting experiments corroborate that Tbr1-positive eminential prethalamic neurons migrate along three streams into hypothalamus, subpallium and septocommissural areas

Abstract

The prethalamic eminence (PThE), a diencephalic caudal neighbor of the telencephalon and alar hypothalamus, is frequently described in mammals and birds as a transient embryonic structure, undetectable in the adult brain. Based on descriptive developmental analysis of Tbr1 gene brain expression in chick embryos, we previously reported that three migratory cellular streams exit the PThE rostralward, targeting multiple sites in the hypothalamus, subpallium and septocommissural area, where eminential cells form distinct nuclei or disperse populations. These conclusions needed experimental corroboration. In this work, we used the homotopic quail-chick chimeric grafting procedure at stages HH10/HH11 to demonstrate by fate-mapping the three predicted tangential migration streams. Some chimeric brains were processed for Tbr1 in situ hybridization, for correlation with our previous approach. Evidence supporting all three postulated migration streams is presented. The results suggested a slight heterochrony among the juxtapeduncular (first), the peripeduncular (next), and the eminentio-septal (last) streams, each of which followed differential routes. A possible effect of such heterochrony on the differential selection of medial to lateral habenular hodologic targets by the migrated neurons is discussed.

Distinct Subdivisions in the Transition Between Telencephalon and Hypothalamus Produce Otp and Sim1 Cells for the Extended Amygdala in Sauropsids

“…A comparison of Sim1 with Foxg1 shows that this area contains Sim1/Foxg1 double-labeled and Sim1 single-labeled cells (present results), indicating an external origin of at least some of the cells of this corridor. Moreover, this ample area also contains Otp cells (part of them coexpressing Foxg1, as noted in the results) and other cell types with different molecular profiles and apparent origins, such as those with Lhx5 and Tbr1 derived from the prethalamic eminence (PThE) and those with Lhx9 of pallial origin (as discussed previously by Abellán et al, 2009 ; see also Abellán and Medina, 2009 ; Abellán et al, 2010 ; Vicario et al, 2017 ; Alonso et al, 2020 , 2021 ). The LOT of mice also appears to include a variety of cell subtypes with different molecular profiles and embryonic origins (discussed by García-López et al, 2008 , Garcia-Calero et al, 2021 ).…”

Analysis of the Expression Pattern of Cajal-Retzius Cell Markers in the <b><i>Xenopus laevis</i></b> Forebrain

“…Recently, it has exhaustively been studied based on the analysis of the marker Tbr1, expressed in mouse and chicken at early and late developing stages [Alonso et al, 2020[Alonso et al, , 2021, as it has been demonstrated in turtle [Moreno et al, 2012], lizard [Desfilis et al, 2018], and Xenopus [Domínguez et al, 2015]. In chicken, three migratory cellular streams have been defined that exit the prethalamic eminence rostralward, targeting multiple sites in the hypothalamus, subpallium, and septocommissural area, where eminential cells form distinct nuclei or disperse populations [Alonso et al, 2021]. Thus, the chicken eminential derivatives seem to respect the telencephalic pallial domains, representing a significant evolutionary difference with respect to the mammalian counterparts [Alonso et al, 2021].…”

“…In chicken, three migratory cellular streams have been defined that exit the prethalamic eminence rostralward, targeting multiple sites in the hypothalamus, subpallium, and septocommissural area, where eminential cells form distinct nuclei or disperse populations [Alonso et al, 2021]. Thus, the chicken eminential derivatives seem to respect the telencephalic pallial domains, representing a significant evolutionary difference with respect to the mammalian counterparts [Alonso et al, 2021]. In reptiles, migratory movements similar to those described in mammals have been suggested on the basis of p73 expression in the prethalamic eminence [Cabrera-Socorro et al, 2007].…”

“…It is frequently described in mammals and birds as a transient embryonic structure, undetectable in the adult brain. Recently, it has exhaustively been studied based on the analysis of the marker Tbr1, expressed in mouse and chicken at early and late developing stages [Alonso et al, 2020[Alonso et al, , 2021, as it has been demonstrated in turtle [Moreno et al, 2012], lizard [Desfilis et al, 2018], and Xenopus [Domínguez et al, 2015]. In chicken, three migratory cellular streams have been defined that exit the prethalamic eminence rostralward, targeting multiple sites in the hypothalamus, subpallium, and septocommissural area, where eminential cells form distinct nuclei or disperse populations [Alonso et al, 2021].…”

“…In amniotes continuity of the prethalamic eminence with the dorsal septum has been observed, questioning the limits between them [Abellán et al, 2010b;Medina and Abellán, 2012] (see discussion in Desfilis et al [2018]). In sauropsids it has been postulated that the dorsal septum, which expresses Lhx5 and Lhx9, could have two parts, based on Lef1 expression [Abellán et al, 2010b;Abellán, 2012, 2014] (see discussion in Desfilis et al [2018]), an intermediate sector expressing Lef1, related to the medial pallium, and another lacking Lef1 [Abellán et al, 2010a[Abellán et al, , 2010b, which might represent a migrated extension of the prethalamic eminence, related to the nucleus of the pallial commissure [Desfilis et al, 2018;Alonso et al, 2020Alonso et al, , 2021. This hypothesis is interesting in line with our results about Zic1/2 expression, both found in the dorsal septum and the prethalamic eminence (present results), which could correspond to this situation.…”