Adult neurogenesis in the brain of the Mozambique tilapia, Oreochromis mossambicus

Abstract

Although the generation of new neurons in the adult nervous system ('adult neurogenesis') has been studied intensively in recent years, little is known about this phenomenon in non-mammalian vertebrates. Here, we examined the generation, migration, and differentiation of new neurons and glial cells in the Mozambique tilapia (Oreochromis mossambicus), a representative of one of the largest vertebrate taxonomic orders, the perciform fish. The vast majority of new cells in the brain are born in specific proliferation zones of the olfactory bulb; the dorsal and ventral telencephalon; the periventricular nucleus of the posterior tuberculum, optic tectum, and nucleus recessi lateralis of the diencephalon; and the valvula cerebelli, corpus cerebelli, and lobus caudalis of the cerebellum. As shown in the olfactory bulb and the lateral part of the valvula cerebelli, some of the young cells migrate from their site of origin to specific target areas. Labeling of mitotic cells with the thymidine analog 5-bromo-2'-deoxyuridine, combined with immunostaining against the neuron-specific marker protein Hu or against the astroglial marker glial fibrillary acidic protein demonstrated differentiation of the adult-born cells into both neurons and glia. Taken together, the present investigation supports the hypothesis that adult neurogenesis is an evolutionarily conserved vertebrate trait.

Spatial distribution and cellular composition of adult brain proliferative zones in the teleost, Gymnotus omarorum

“…This is in agreement with the results reported in A. leptorhynchus, O. latipes, N. Furzeri, A. burtoni , and O. mossambicus , (Zupanc and Horschke, 1995; Kuroyanagi et al, 2010; Terzibasi et al, 2012; Maruska et al, 2012; Teles et al, 2012) and D. rerio (Zupanc et al, 2005; Zupanc, 2011). However, according to Adolf et al (2006) and Grandel et al (2006) this proliferation zone in D. rerio is restricted to the ventral portion of the diencephalic ventricle.…”

“…Very scarce proliferating cells were found in the OB of adult G. omarorum , most of which were located within the glomerular layer or at the dorsal-medial surface of the intermediate zone of the OB (corresponding to the rostralmost region of the telencephalic ventricle). This is consistent with the results reported in D. rerio (Byrd and Brunjes, 2001; Adolf et al, 2006; Grandel et al, 2006; Zupanc, 2011), A. burtoni (Maruska et al, 2012), and O. mossambicus (Teles et al, 2012). Conversely, Ekström et al (2001) reported proliferating cells at the internal cell layer of G. aculeatus , and Fernández et al (2011) found labeled cells in all OB laminae of Austrolebias (with the highest long term thymidine label retaining cells concentration in its medial and rostral part.…”

“…Proliferating cells were distributed all along the extension of the ventricular lining of the telencephalon in G. omarorum , with a prominent proliferation zone adjacent to the subpallium, similar to G. aculeatus (Ekström et al, 2001), D. rerio (Adolf et al, 2006; Grandel et al, 2006; Zupanc, 2011), O. bonariensis (Strobl-Mazzulla et al, 2010), A. burtoni (Maruska et al, 2012), O. mossambicus (Teles et al, 2012), A. leptorhynchus (in which the dorsal-lateral telencephalic division showed the largest amount of proliferating cells; Zupanc and Horschke, 1995), and O. latipes (Kuroyanagi et al, 2010). Very scarce proliferating cells were found in the OB of adult G. omarorum , most of which were located within the glomerular layer or at the dorsal-medial surface of the intermediate zone of the OB (corresponding to the rostralmost region of the telencephalic ventricle).…”

“…Among teleosts, adult cell proliferation and neurogenesis have been thoroughly characterized in wave type weakly electric gymnotids, particularly in Apteronotus leptorhynchus [ A. leptorhynchus : (Zupanc and Horschke, 1995; Zupanc et al, 1996; Zupanc, 2001; Hinsch and Zupanc, 2006); Eigenmannia sp: (Zupanc and Zupanc, 1992); and Brachyhypopomus gauderio : (Dunlap et al, 2011)]. The spatial distribution of brain proliferation zones in adult wave type weakly electric gymnotids roughly resembles that of other teleosts [ Astatotilapia burtoni (Maruska et al, 2012); Austrolebias (Fernández et al, 2011); Carassius auratus (Raymond and Easter, 1983; Delgado and Schmachtenberg, 2011); Danio rerio (Maeyama and Nakayasu, 2000; Zupanc et al, 2005; Adolf et al, 2006; Grandel et al, 2006; Ampatzis and Dermon, 2007; Kaslin et al, 2009; Ito et al, 2010; März et al, 2010; Zupanc, 2011); Gasterosteus aculeatus (Ekström et al, 2001); Nothobranchius furzeri (Terzibasi et al, 2012); Odontesthes bonariensis (Strobl-Mazzulla et al, 2010); Oreochromis mossambicus (Teles et al, 2012); Oryzias latipes (Nguyen et al, 1999; Candal et al, 2005a; Alunni et al, 2010; Kuroyanagi et al, 2010; Isoe et al, 2012) and Salmo trutta fario (Candal et al, 2005b)], despite the phylogenetic distance to most of those species. However, differences have been observed that were attributed to the functional specialization of weakly electric fish (Zupanc and Horschke, 1995; Grandel et al, 2006; Grandel and Brand, 2013).…”

Expression of a novel serine/threonine kinase gene, Ulk4, in neural progenitors during Xenopus laevis forebrain development

“…Currently, it is known that in mammals, adult neurogenesis takes place only in a few areas (Eriksson et al, 1998;Gould et al, 1999;Peretto et al, 1999;Lee and Blackshaw, 2012) while numerous studies have reported widespread neurogenesis in non-mammals such as fish (Zikopoulos et al, 2001;Zupanc et al, 2005;Grandel et al, 2006;Ampatzis and Dermon, 2007;Teles et al, 2012), amphibians (Richter and Kranz, 1981;Simmons et al, 2008;D'Amico et al, 2013), reptiles (Lo´pez-Garcı´a et al, 1988, 1990DelgadoGonza´lez et al, 2011) and birds (Scharff et al, 2000). In this context, very recent studies have described a new germinative zone in the adult mammalian brain, located in the hypothalamic region (Kokoeva et al, 2005;Lee and Blackshaw, 2012;Cheng, 2013), in agreement with what was found in amphibians (Simmons et al, 2008).…”