Gene expression analysis of developing cell groups in the pretectal region of Xenopus laevis

Abstract

Our previous analysis of progenitor domains in the pretectum of Xenopus revealed three molecularly distinct anteroposterior subdivisions, identified as precommissural (PcP), juxtacommissural (JcP), and commissural (CoP) histogenetic domains (Morona et al. [2011] J Comp Neurol 519:1024-1050). Here we analyzed at later developmental stages the nuclei derived from these areas, attending to their gene expression patterns and histogenesis. Transcription-factor gene markers were used to selectively map derivatives of each domain: Pax7 and Pax6 (CoP); Foxp1 and Six3 (JcP); and Xiro1, VGlut2, Ebf1, and Ebf3 (PcP). Additional genoarchitectural information was provided by the expression of Gbx2, NPY, Lhx1, and Lhx9. This allowed both unambiguous characterization of the anuran pretectal nuclei with regard to their origin in the three early anteroposterior progenitor domains, and their comparison with counterparts in the chick and mouse pretectum. Our observations demonstrated a molecular conservation, during practically all the stages analyzed, for most of the main markers used to define genoarchitecturally the main derivatives of each pretectal domain. We found molecular evidence to propose homologous derivatives from the CoP (olivary pretectal, parvocellular, and magnocellular posterior commissure and lateral terminal nuclei), JcP (spiriformis lateral and lateral terminal nuclei), and PcP (anterior pretectal nucleus) to those described in avian studies. These results represent significant progress in the comprehension of the diencephalic region of Xenopus and show that the organization of the pretectum possesses many features shared with birds. J. Comp. Neurol. 525:715-752, 2017. © 2016 Wiley Periodicals, Inc.

Genoarchitecture of the Early Postmitotic Pretectum and the Role of Wnt Signaling in Shaping Pretectal Neurochemical Anatomy in Zebrafish

“…Our analysis shows that the neurochemical anatomy of the pretectum is evolutionarily conserved, with the PcP being primarily glutamatergic with a presence of GABAergic cells in outer intermediate and superficial strata (summarized in Figure 8). The JcP highlighted their gad1b content, and the CoP showed clusters of neurons of both gad1b and vglut2.2 identities in zebrafish as was observed in previously analyzed Xenopus laevis and mice (Morona et al, 2011(Morona et al, , 2017Virolainen et al, 2012). The clusters of strongly immunoreactive cells extended dorsoventrally, as previously described for 48 hpf zebrafish and 4 dpf Gasterosteus aculeatus (Ekström and Ohlin, 1995;Mueller et al, 2006).…”

“…However, this zebrafish region is poorly characterized after this stage to the final anatomical organization in the adult. Pioneering studies on the pretectal region of birds and Xenopus laevis that cover different stages of development indicate that an adequate characterization in the adult requires an exhaustive interpretation of the processes that occur during the different stages of development (Ferran et al, 2007(Ferran et al, , 2009Merchán et al, 2011;Morona et al, 2011Morona et al, , 2017. Here, we studied the development of the pretectum in zebrafish, focusing on the early post-neurogenesis stage.…”

“…These studies described evolutionarily conserved rostrocaudal progenitor domains of the pretectal region, named according to their relative positions to the posterior commissure: the precommissural (PcP), the juxtacommissural pretectum (JcP) and the commissural (CoP) pretectum (Redies, 2000;Ferran et al, 2007Ferran et al, , 2008Lauter et al, 2013). The prosomeric model has also been applied to analyze pretectal regionalization during the early postmitotic and later stages of pretectal nuclei formation in Xenopus laevis, chicks, and quail, enabling attempts to link the origin of pretectal derivatives from developmental subdomains to the mature nuclei (Ferran et al, 2007(Ferran et al, , 2009Merchán et al, 2011;Morona et al, 2011Morona et al, , 2017. Although zebrafish is a popular model in neuroresearch, the development of its pretectum was poorly investigated at this stage, and the relationship between the progenitor domains and the mature pretectal nuclei remains enigmatic.…”

The nucleus pretectalis principalis: A pretectal structure hidden in the mammalian thalamus

“…In toads and frogs the caudal dorsal part of the so-called lateral thalamic nucleus contains NPY-ir cells that project bilaterally to the TeO (Chapman & Debski, 1995;Kozicz & Lazar, 1994). A recent characterization of the genoarchitecture of the xenopus pretectum further supports the existence of an amphibian PT (Morona, Ferran, & Puelles, 2016). In fish and agnathan species, the evidence for a PT is more elusive but consistent.…”

Wilhelm His’ lasting insights into hindbrain and cranial ganglia development and evolution

“…The autonomy of ingrowing afferents suggests that the developmental formation of epibranchial and dorsolateral placode-derived sensory neurons and afferent projections precedes the formation of distinct target nuclei in the hindbrain, much as the formation of specific areas of neuropil precedes formation of distinct nuclei in the visual system (Herrick 1948; Rettig et al 1981; Morona et al 2017). This accords somewhat with the neurobiotactic idea of Ariens-Kappers (Kappers et al 1936) that central neurons migrate into areas of their major sensory input and thus generate sensory ‘nuclei’.…”