Adult Neurogenesis in the Hedgehog (Erinaceus concolor) and Mole (Talpa europaea)

Abstract

We investigated adult neurogenesis in two species of mammals belonging to the superorder Laurasiatheria, the southern white-breasted hedgehog (order Erinaceomorpha, species Erinaceus concolor) from Armenia and the European mole (order Soricomorpha, species Talpa europaea) from Poland. Neurogenesis in the brain of these species was examined immunohistochemically, using the endogenous markers doublecortin (DCX) and Ki-67, which are highly conserved among species. We found that in both the hedgehog and mole, like in the majority of earlier investigated mammals, neurogenesis continues in the subventricular zone (SVZ) of the lateral ventricles and in the dentate gyrus (DG). In the DG of both species, DCX-expressing cells and Ki-67-labeled cells were present in the subgranular and granular layers. In the mole, a strong bundle of DCX-labeled processes, presumably axons of granule cells, was observed in the center of the hilus. Proliferating cells (expressing Ki-67) were identified in the SVZ of lateral ventricles of both species, but neuronal precursor cells (expressing DCX) were also observed in the olfactory bulb (OB). In both species, the vast majority of cells expressing DCX in the OB were granule cells with radially orientated dendrites, although some periglomerular cells surrounding the glomeruli were also labeled. In addition, this paper is the first to show DCX-labeled fibers in the anterior commissure of the hedgehog and mole. These fibers must be axons of new neurons making interhemispheric connections between the two OB or piriform (olfactory) cortices. DCX-expressing neurons were observed in the striatum and piriform cortex of both hedgehog and mole. We postulate that in both species a fraction of cells newly generated in the SVZ migrates along the rostral migratory stream to the piriform cortex. This pattern of migration resembles that of the ‘second-wave neurons’ generated during embryonal development of the neocortex rather than the pattern observed during development of the allocortex. In spite of the presence of glial cells alongside DCX-expressing cells, we never found colocalization of DCX protein with a glial marker (vimentin or glial fibrillary acidic protein).

The Distribution of Doublecortin-Immunopositive Cells in the Brains of Four Afrotherian Mammals: the Hottentot Golden Mole <b><i>(Amblysomus hottentotus)</i></b>, the Rock Hyrax <b><i>(Procavia capensis)</i></b>, the Eastern Rock Sengi <b><i>(Elephantulus myurus)</i></b> and the Four-Toed Sengi <b><i>(Petrodromus tetradactylus)</i></b>

“…From the periventricular layer of the OB, these new neurons migrate radially into the granular and glomerular layers where they become functionally integrated into the OB circuitry [Peretto et al, 1997;Bedard and Parent, 2004;Lledo et al, 2006]. This continuous supply of new neurons to the OB has been reported in all mammalian species studied to date, including the four afrotherian species studied herein [Pencea et al, 2001;Bedard et al, 2002;Bedard and Parent, 2004;Alpár et al, 2010;Bartkowska et al, 2010;Ngwenya et al, 2011;Patzke et al, 2013a, b]; however, this rostral migration seems to be absent in humans [Eriksson et al, 1998;Bergmann et al, 2012], with some studies suggesting that newly generated neurons in the human OB are generated locally [Bedard and Parent, 2004].…”

“…DCX is a microtubule-associated phosphoprotein that is expressed from 2 weeks up to 6 months in actively dividing neuronal precursor cells and their neuronal daughter cells [Brown et al, 2003;Rao and Shetty, 2004;Kohler et al, 2011]. The use of DCX as a marker is Patzke et al Brain Behav Evol 2014;84:227-241 DOI: 10.1159/000367934 230 advantageous in that it minimises pre-handling of animals while providing an average rate of expression of new neurons in natural conditions prior to capture of the animal [Bartkowska et al, 2010]. Goat anti-DCX (C-18; Santa Cruz Biotechnology, Dallas, Tex., USA) was used to visualise DCX, as this antibody has been previously demonstrated to provide distinct labelling in rodents, humans and other mammals [Brown et al, 2003;Liu et al, 2008;Ngwenya et al, 2011;Patzke et al, 2013a, b].…”

Adult Hippocampal Neurogenesis in Natural Populations of Mammals

“…In the order of Eulipotyphla (the taxonomic order comprising most of the former insectivores), AHN has been shown using Ki67 and I. Amrein DCX in wild European moles (Talpa europaea) and hedgehogs (Erinaceus concolor [Bartkowska et al 2010]) and with BrdU in combination with NeuN in wild common and pygmy shrews (Sorex araneus and Sorex minutus [Bartkowska et al 2008]). The number of proliferating cells in moles and hedgehogs appear rather low in comparison to rodent data; total granule cell number was, however, not assessed, and a quantitative comparison is therefore difficult.…”

Typical and atypical stem cells in the brain, vitamin C effect and neuropathology

“…Neurotrophin 3 (NT3), a factor expressed in the ventricular zone, has also been implicated in neurogenesis (Ohtsuka et al, 2009). Once NT3 is released to the extracellular medium, it activates the ERK1/2 signaling pathway, which ultimately leads to the activation of transcription factors that control neuronal diff erentiation (Bartkowska et al, 2010;Ohtsuka et al, 2009).…”