Postembryonic development of the cerebellum in gymnotiform fish

Abstract

In contrast to adult mammals, adult teleost fish regularly generate new neurons and glial cells in many brain regions. A previous quantitative mapping of the proliferation zones in the brain of adult Apteronotus leptorhynchus (Teleostei, Gymnotiformes) has shown that 75% of all mitotically active cells are situated in the cerebellum (Zupanc and Horschke [1995] J. Comp. Neurol. 353:213-233). By employing the thymidine analogue 5-bromo-2'-deoxyuridine, we have, in the present study, investigated the postembryonic development of this brain region in detail. In the corpus cerebelli and the valvula cerebelli, the vast majority of newborn cells originate in the respective molecular layers. Within the first few days of their life, these cells migrate toward specific target areas, namely, the respective granule cell layers. In the caudal part of the cerebellum, the granule cell layer of the eminentia granularis pars medialis displays the highest mitotic activity. From there, the cells migrate through the adjacent molecular layer to the granule cell layer of the eminentia granularis pars posterior. Combination of retrograde-tracing techniques with immunohistochemistry for 5-bromo-2'-deoxyuridine showed that at least a portion of the newly generated cells develop into granule neurons. Many of the newly generated cells survive for long periods of time. A large fraction of these cells is added to the population of already existing cells, thus resulting in a permanent growth of the target areas and their associated structures.

Quantitative genetic analysis of brain size variation in sticklebacks: support for the mosaic model of brain evolution

“…Relatively high heritability estimates of total brain size have also been reported from other primate species [50,51], rodents [18,19] and birds [21]. However, these are all taxa with determinate growth, whereas fishes exhibit indeterminate growth and neurogenesis that continues throughout life in all parts of the brain [52,53]. Hence, the relative contribution of environmental influences on fish brain architecture may exceed that seen in vertebrate taxa with determinate growth.…”

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

“…A schematic diagram of each section was drawn using Inkscape, and the location of actively cells cycling (4 and 24 h after thymidine analog administration) and long term weak thymidine analog label retaining cells were represented by red and blue dots, respectively. The nomenclature and abbreviations used in this article to describe the location of brain proliferation zones in G. omarorum correspond to those used by Maler et al (1991), Zupanc et al (1996) and Meek and Nieuwenhuys (1998). …”

“…Whereas in adult mammals in vivo neurogenesis occurs in two brain regions, the subventricular zone of the lateral ventricle (SVZ) and the subgranular zone of the hippocampal dentate gyrus (Altman and Das, 1965; Altman, 1969, 2011), in adult teleosts it occurs not only in their homologous structures but also in several other regions of all brain divisions (Lindsey and Tropepe, 2006; Zupanc, 2006, 2008; Chapouton et al, 2007; Kaslin et al, 2008; Grandel and Brand, 2013). 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.…”

Stretching the limits: Stem cells in regeneration science

“…These new cells originate from pluripotent adult stem cells harbored in dozens of specific proliferation zones within the brain (Hinsch and Zupanc, 2006). Approximately half of the new cells persist for the rest of the fish's life and develop into a variety of cell types, including neurons and glial cells (Zupanc et al, 1996(Zupanc et al, , 2005Ott et al, 1997;Hinsch and Zupanc, 2007).…”