Abstract
Expression patterns of Nkx2.1 and Islet-1 (Isl1), which encode transcription factors that are key in the regionalization of the forebrain, were analyzed by combined immunohistochemical methods in young adult specimens of two lungfishes (Neoceratodus forsteri and Protopterus dolloi) and a urodele amphibian (Pleurodeles waltl). We aimed to get insights into the possible organization of the forebrain in the common ancestor of all tetrapods because of the pivotal phylogenetic significance of these two groups, being lungfishes the closest living relatives of tetrapods, and representing urodeles a model of simple brain organization with most shared features with amniotes. These transcription factors display regionally restricted expression domains in adult (juvenile) brains that are best interpreted according to the current prosomeric model. The regional patterns observed serve to identify regions and compare between the three species studied, and with previous data reported mainly for amniotes. We corroborate that Nkx2.1 and Isl1 expressions have very similar topologies in the forebrain. Common features in all sarcopterygians (lungfishes and tetrapods) have been observed, such as the Isl1 expression in most striatal neurons, whereas Nkx2.1 is restricted to migrated interneurons that reach the ventral pallium (VP). In the pallidal derivatives, the combination of both markers allows the identification of the boundaries between the ventral septum, the bed nucleus of the stria terminalis (BST) and the preoptic commissural region. In addition, the high Isl1 expression in the central amygdala (CeA), its boundary with the lateral amygdala (LA), and the scattered Nkx2.1 expression in the medial amygdala (MeA) are also shared features. The alar and basal hypothalamic territories, and the prethalamus and posterior tubercle (TP) in the diencephalon, have maintained a common pattern of expression. This regional distribution of Isl1 and Nkx2.1 observed in the forebrain of urodeles and lungfishes contributes further to our understanding of the first terrestrial vertebrates and their ancestors.
Highlights
Developmental processes occurring from the neural plate stages entail drastic morphological changes and the topological arrangement of the forebrain subdivisions is a consequence of the location of their primordia in the neural plate
We will deal with the main regions of the forebrain comparatively, and major traits of expression will be detailed for the urodele and the lungfish species
In other vertebrates the main body of the lateral ganglionic eminence (LGE) that will give rise to the striatal projection neurons is the one with intense Isl1 expression but a second small dorsal territory lacks Isl1 cells (Stenman et al, 2003; Moreno et al, 2009) and our observations suggest that it is a highly conserved condition in evolution, shared by all the vertebrates studied
Summary
Developmental processes occurring from the neural plate stages entail drastic morphological changes and the topological arrangement of the forebrain subdivisions is a consequence of the location of their primordia in the neural plate This organization is driven by the combination of basic genetic codes, which are strongly conserved in the different animal models, and the mechanisms leading to the formation and patterning of the brain are highly conserved in evolution. Many shared features have been reported in the forebrain organization across tetrapods, and an interesting issue to resolve in evolutionary terms would be to understand the organization of the forebrain of early tetrapods. To this aim, we have selected two representative groups. In early comparative neuroanatomy the brain of urodeles was chosen to focus on the species with the simplest brains (Herrick, 1948), because salamanders were easier to obtain and work with than lepidosirenid brains
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