Amphibian thalamic nuclear organization during larval development and in the adult frog Xenopus laevis: Genoarchitecture and hodological analysis

Abstract

The early patterning of the thalamus during embryonic development defines rostral and caudal progenitor domains, which are conserved from fishes to mammals. However, the subsequent developmental mechanisms that lead to the adult thalamic configuration have only been investigated for mammals and other amniotes. In this study, we have analyzed in the anuran amphibian Xenopus laevis (an anamniote vertebrate), through larval and postmetamorphic development, the progressive regional expression of specific markers for the rostral (GABA, GAD67, Lhx1, and Nkx2.2) and caudal (Gbx2, VGlut2, Lhx2, Lhx9, and Sox2) domains. In addition, the regional distributions at different developmental stages of other markers such as calcium binding proteins and neuropeptides, helped the identification of thalamic nuclei. It was observed that the two embryonic domains were progressively specified and compartmentalized during premetamorphosis, and cell subpopulations characterized by particular gene expression combinations were located in periventricular, intermediate and superficial strata. During prometamorphosis, three dorsoventral tiers formed from the caudal domain and most pronuclei were defined, which were modified into the definitive nuclear configuration through the metamorphic climax. Mixed cell populations originated from the rostral and caudal domains constitute most of the final nuclei and allowed us to propose additional subdivisions in the adult thalamus, whose main afferent and efferent connections were assessed by tracing techniques under in vitro conditions. This study corroborates shared features of early gene expression patterns in the thalamus between Xenopus and mouse, however, the dynamic changes in gene expression observed at later stages in the amphibian support mechanisms different from those of mammals.

Neural origins of basal diencephalon in teleost fishes: Radial versus tangential migration

“…Mechanisms of Development, 117. Abbreviations: DiVe, diencephalic ventricle; fr, fasciculus retroflexus; Hv, ventral zone of periventricular hypothalamus; M2, larval preglomerular complex; mfb, medial forebrain bundle; PG, preglomerular complex; PGa, anterior nucleus of PG; PGl, lateral nucleus of PG; PPr, periventricular pretectum; prtf, pretectal retinal terminal field; PVO, paraventricular organ; SP, superficial pretectum; TeO, tectum opticum; TecVe, tectal ventricle; Th, (dorsal) thalamus; TH, tuberal hypothalamus; TLa, lateral torus; TLo, torus longitudinalis; TPp, periventricular nucleus of posterior tuberculum; ZLI, zona limitans intrathalamica [Color figure can be viewed at wileyonlinelibrary.com] species examined and compare even easily to cartilaginous fishes and amphibians (see, e.g., the recent paper on the frog thalamus; Morona, Bandín, López, Moreno, & González, 2020), there is great diversity in pretectal, preglomerular, or lateral hypothalamic regions (inferior lobe) ( Figure 2). These areas greatly vary in teleosts depending on sensory specializations and show tremendous species or taxon-specific differences in size (note bars in Figure 2) and nuclear composition.…”

“…In contrast, the extensive lateral posterior tubercular area in teleosts lacks dopaminergic and other monoaminergic neurons, but it is dominated instead by various nuclei concerned with ascending sensory circuitry in the form of the teleostean‐typical, so‐called preglomerular complex. Whereas the dorsal and ventral thalami are conservative in neuroanatomical appearance within most teleost species examined and compare even easily to cartilaginous fishes and amphibians (see, e.g., the recent paper on the frog thalamus; Morona, Bandín, López, Moreno, & González, 2020), there is great diversity in pretectal, preglomerular, or lateral hypothalamic regions (inferior lobe) (Figure 2). These areas greatly vary in teleosts depending on sensory specializations and show tremendous species or taxon‐specific differences in size (note bars in Figure 2) and nuclear composition.…”

Analysis of Islet‐1, Nkx2.1, Pax6, and Orthopedia in the forebrain of the sturgeon Acipenser ruthenus identifies conserved prosomeric characteristics

“…Increasing evidence supports a prosomerically organized ground plan (or bauplan) of the vertebrate brain (for basic literature, see Puelles & Rubenstein, 2015;Puelles, 2019). Specifically, conserved expression patterns of gene-regulatory genes like Islet-1 (Isl1), Nkx2.1, Orthopedia (Otp), and Pax6 support the identification of homologous forebrain regions (Bandín et al, 2014;Domínguez et al, 2014Domínguez et al, , 2015Joven et al, 2013aJoven et al, , 2013bMorales-Delgado et al, 2011;Moreno et al, , 2014Moreno et al, , 2018Morona et al, 2020;Santos-Durán et al, 2015).…”

Xenopus leads the way: Frogs as a pioneering model to understand the human brain

“…Indeed, canonical forebrain markers exhibit conserved expression patterns in Xenopus and mammalian brains (Figure 4). As development and conservation of several regions of the diencephalon have been recently highlighted (Bandín et al, 2015; Domínguez, González, & Moreno, 2014; Domínguez, González, & Moreno, 2015; Domínguez, Morona, González, & Moreno, 2013; Moreno & González, 2020; Moreno, Morona, López, & González, 2017; Morona, Bandín, López, Moreno, & González, 2020), we will restrict the present discussion to the telencephalon. Within the developing foxg1 + telencephalon (Figure 2), the subpallium expresses nkx2.1 , isl1 , ascl1 , dlx2/5 , gsx1/2 (Bachy, Berthon, & Rétaux, 2002; Brox, Ferreiro, Puelles, & Medina, 2002; Brox, Puelles, Ferreiro, & Medina, 2003; Hollemann & Pieler, 2000; Illes, Winterbottom, & Isaacs, 2009; Moreno, Domínguez, Rétaux, & González, 2008; Papalopulu & Kintner, 1993; Small, Vokes, Garriock, Li, & Krieg, 2000; van den Akker, Brox, Puelles, Durston, & Medina, 2008; Winterbottom, Illes, Faas, & Isaacs, 2010) while the pallium is marked by the expression of pax6 , emx1/2 , ngn , neuroD , and tbr1/2 (Bachy et al, 2002; Brox, Puelles, Ferreiro, & Medina, 2004; D'Amico et al, 2013; Fernandez et al, 1998; Hirsch & Harris, 1997; Pannese et al, 1998; Ryan, Butler, Bellefroid, & Gurdon, 1998; Wullimann et al, 2005).…”

“…Indeed, canonical forebrain markers exhibit conserved expression patterns in Xenopus and mammalian brains (Figure 4). As development and conservation of several regions of the diencephalon have been recently highlighted (Bandín et al, 2015;Domínguez, González, & Moreno, 2014;Domínguez, González, & Moreno, 2015;Domínguez, Morona, González, & Moreno, 2013;Moreno, Morona, López, & González, 2017;Morona, Bandín, López, Moreno, & González, 2020), we will restrict the present discussion to the telencephalon. Within the developing foxg1+ telencephalon (Figure 2), the subpallium expresses nkx2.…”