Comparative Analysis of Nkx2.1 and Islet-1 Expression in Urodele Amphibians and Lungfishes Highlights the Pattern of Forebrain Organization in Early Tetrapods

Ventralization, a major patterning process in the developing vertebrate neural tube (central nervous system, CNS), depends on Sonic hedgehog (SHH) as a main signaling morphogen. We studied the CNS of late larval and young adult zebrafish in a transgenic shh‐GFP line revealing increased neuroanatomical detail due to the progressed differentiation state compared to earlier stages. Some major findings emerge from the present study. (a) shh –GFP is still expressed along the adult zebrafish CNS neuraxis in most locations seen in larvae. (b) We newly identify a ventroposterior shh pallidal domain representing the basal telencephalic signaling center important for basal ganglia development known in other vertebrates (i.e., the anterior entopeduncular area—basal medial ganglionic eminence of mammals). (c) We further show late‐emerging shh‐GFP positive radial glia cells in the medial zone of the dorsal telencephalon (i.e., the teleostan pallial amygdala). (d) Immunostains for tyrosine hydroxylase demonstrate that there is selective colocalization in adult dopamine cells with shh‐GFP in the posterior tuberculum, including in projection cells to striatum, which represents a striking parallel to amniote mesodiencephalic dopamine cell origin from shh expressing floor plate cells. (e) There is no colocalization of shh and islet1 as shown by respective shh‐GFP and islet1‐GFP lines. (f) The only radially far migrated shh‐GFP cells are located in the preglomerular area. (g) There are no adult cerebellar and tectal shh‐GFP cells confirming their exclusive role during early development as previously reported by our laboratory.

Section: Discussionmentioning

confidence: 80%

“…In addition to this information in amniotes, a similar situation is present in basal anamniote sarcopterygians (frogs, salamanders, and Domínguez, Rétaux, & González, 2008;Moreno et al, 2018), as well as regarding the process of tangential migration .…”

Section: What Is the Role Of Shh In Telencephalic Gene Expression Imentioning

confidence: 73%

Sonic hedgehog expression in zebrafish forebrain identifies the teleostean pallidal signaling center and shows preglomerular complex and posterior tubercular dopamine cells to arise from shh cells

Wullimann

Umeasalugo

2019

Section: Discussionmentioning

confidence: 99%

“…Therefore, the presence of a prethalamic dopaminergic population seems to be a conserved feature in the evolution of DA system. Interestingly, in mammals, the expression of the genes Arx and Isl1 is required for the development of prethalamic dopaminergic cells (Filippi, Jainok, & Driever, 2012), and Isl1 is strongly expressed in the prethalamus of cladistians (personal observation) like in amphibians and lungfishes (Moreno et al, 2018;Moreno, Domínguez, Rétaux, & González, 2008 The most conspicuous dopaminergic cell population in the diencephalon of cladistians is situated in the posterior tubercle, within the basal part of p3, similarly to the observations reported in teleosts (Bhat & Ganesh, 2017;Forlano & Sisneros, 2016;Karoubi et al, 2016;Rink & Wullimann, 2001, 2002a, 2002bRyczko et al, 2016;, and other groups of fishes as chondrosteans (Adrio et al, 2002), elasmobranchs (Carrera et al, 2012;Molist et al, 1993), and lampreys (Pierre et al, 1997;Pombal et al, 1997). The amphibians also present a remarkable TH/DA-ir cell population in the posterior tubercle , whereas in lungfishes this dopaminergic group is less developed (López & González, 2017).…”

Section: Diencephalonmentioning

confidence: 99%

Organization of the catecholaminergic systems in two basal actinopterygian fishes, Polypterus senegalus and Erpetoichthys calabaricus (Actinopterygii: Cladistia)

López

Lozano

Morona

et al. 2018

Self Cite

Cladistians are a group of basal nonteleost actinopterygian fishes that represent an interesting group for the study of primitive brain features, most likely present in the ancestral Osteichthyes. We have investigated the catecholaminergic (CA) systems in the brain of two representative cladistian species, the bichir Polypterus senegalus and the reedfish Erpetoichthys calabaricus, by means of antibodies against tyrosine hydroxylase (TH; the first enzyme in the synthesis of catecholamines) and dopamine (DA). Double immunohistofluorescence was performed for simultaneous detection of TH with nitric oxide synthase, choline acetyltransferase, calbindin, calretinin, and serotonin, aiming to accurately establish the localization of the CA neurons and to assess possible interactions between these neuroactive substances. All forebrain CA groups of cladistians are dopaminergic, whereas noradrenergic cells are located within the rhombencephalon. Distinct groups of DA immunoreactive (DA‐ir) cells were observed in the olfactory bulb, subpallium, and preoptic area of the telencephalon. Hypothalamic groups were detected in the suprachiasmatic nucleus, retrotuberal and retromamillary areas and, in particular, the paraventricular organ showed immunoreactivity to dopamine but not to TH. Diencephalic DA‐ir groups were detected in the prethalamus, posterior tubercle, and pretectum. A small DA‐ir cell population was observed in the midbrain tegmentum only in Polypterus. CA cell groups were also located in the locus coeruleus, solitary tract nucleus, and area postrema within the rhombencephalon, the spinal cord, and the retina. The comparison of these results with other vertebrates, using a neuromeric analysis, shows highly conserved traits in all vertebrates studied but also evidences particular characteristics of actinopterygian fishes.

“…Actually, their neuroanatomical organization is of special interest for deducing evolutionary traits in the brain that were conserved, modified, or lost in the transition from fishes to land vertebrates. Thus, many features observed in living lungfishes may resemble those of ancestral tetrapods in the evolution from an aquatic fish ancestor (see Moreno et al, ). In spite of their important phylogenetic position, there are relatively few studies on the neuroanatomy of lungfishes using specific and more modern methods like immunohistochemistry, in situ hybridization, or tract‐tracing techniques (see López, Morona, Moreno, & González, ; Morona, López, Northcutt, & González, ).…”

Section: Introductionmentioning

confidence: 99%

Pattern of nitrergic cells and fibers organization in the central nervous system of the Australian lungfish,Neoceratodus forsteri(Sarcopterygii: Dipnoi)

López

Morona

González

2019

Self Cite

The Australian lungfish Neoceratodus forsteri is the only extant species of the order Ceratodontiformes, which retained most of the primitive features of ancient lobe finned‐fishes. Lungfishes are the closest living relatives of land vertebrates and their study is important for deducing the neural traits that were conserved, modified, or lost with the transition from fishes to land vertebrates. We have investigated the nitrergic system with neural nitric oxide synthase (NOS) immunohistochemistry and NADPH‐diaphorase (NADPH‐d) histochemistry, which yielded almost identical results except for the primary olfactory projections and the terminal and preoptic nerve fibers labeled only for NADPH‐d. Combined immunohistochemistry was used for simultaneous detection of NOS with catecholaminergic, cholinergic, and serotonergic structures, aiming to establish accurately the localization of the nitrergic elements and to assess possible interactions between these neurotransmitter systems. The results demonstrated abundant nitrergic cells in the basal ganglia, amygdaloid complex, preoptic area, basal hypothalamus, mesencephalic tectum and tegmentum, laterodorsal tegmental nucleus, reticular formation, spinal cord, and retina. In addition, low numbers of nitrergic cells were observed in the olfactory bulb, all pallial divisions, lateral septum, suprachiasmatic nucleus, prethalamic and thalamic areas, posterior tubercle, pretectum, torus semicircularis, cerebellar nucleus, interpeduncular nucleus, the medial octavolateral nucleus, nucleus of the solitary tract, and the dorsal column nucleus. Colocalization of NOS and tyrosine hydroxylase was observed in numerous cells of the ventral tegmental area/substantia nigra complex. Comparison with other vertebrates, using a neuromeric analysis, reveals that the nitrergic system of Neoceratodus shares many neuroanatomical features with tetrapods and particularly with amphibians.