A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum

Abstract

Protracted neurogenesis occurs at different postnatal stages in different brain locations, whereby leading to site-specific adult neurogenesis in some cases. No spontaneous genesis of neurons occurs in the cerebellum after the postnatal genesis of granule cells from the external germinal layer (EGL), a transitory actively proliferating zone which is thought to be exhausted before puberty. Here, we show the protracted genesis of newly generated neuronal precursors in the cerebellar cortex of young rabbits, persisting beyond puberty. Neuroblasts generated within an actively proliferating subpial layer thus extending the postnatal EGL are arranged to form thousands of tangential chains reminiscent of those responsible for cell migration in the forebrain subventricular zone. These subpial chains cover the whole cerebellar surface from the 2nd to the 5th month of life, then disappearing after puberty. In addition, we describe the appearance of similar groups of cells at the end of granule cell genesis in the mouse cerebellum, here limited to the short period of EGL exhaustion (4-5 days). These results show common features do exist in the postnatal reorganization of secondary germinal layers of brain and cerebellum at specific stages, parallel to differences in the slowing down of cerebellar neurogenesis among mammalian species.

Noncanonical Sites of Adult Neurogenesis in the Mammalian Brain

“…Still in rabbits, the combination of cell proliferation markers, detected at different postinjection survival times, with DCX and PSA-NCAM staining revealed a parenchymal genesis of Pax2 þ interneurons in the cerebellar cortex, resulting from further proliferation of cells of neuroepithelial origin ). This process shows features of both delayed neurogenesis, extending until and around puberty (Ponti et al 2006b), and persistent neurogenesis occurring, to a lesser extent, during adulthood . Thus, in the striatal and cerebellar parenchyma of lagomorphs, in sharp contrast with our common knowledge concerning the CNS of other mammals, new neurons are spontaneously generated independently from remnants of germinal layers, yet their final outcome, possible integration, and role in the adult neural circuits remains obscure.…”

“…Recent studies revealed that protracted cerebellar neurogenesis extends around and beyond puberty in the New Zealand white rabbit (Ponti et al 2006b), then persisting, to a lesser extent, during adulthood in the absence of germinal layers (Ponti et al , 2010. Thus, unlike other mammals, in lagomorphs an overlapping of protracted (germinal-layer derived) and adult ( parenchymal) cerebellar neurogenesis do occur.…”

Polysialyltransferase expression is linked to neuronal migration in the developing and adult zebrafish

“…It has been shown to be involved in regulating embryonic neurogenesis (Ponti et al, 2006), neuronal migration (Ono et al, 1994;Wang et al, 1994;Hu et al, 1996), axonal pathfinding (Tang et al, 1992;Daston et al, 1996;Cremer et al, 1997;Marx et al, 2001), as well as synaptogenesis (Seki and Rutishauser, 1998). Furthermore, in the mature brain, NCAM has been implicated in regulating adult neurogenesis (Vutskits et al, 2006), neuronal migration (Cremer et al, 1994), survival of neural stem cell derived neuronal progenitors (Gascon et al, 2007), synaptic plasticity, and learning (Becker et al, 1996;Muller et al, 1996).…”

Subclavian steal syndrome decreases neurogenesis in the cerebellar cortex and affects cognitive function in rabbits

“…The SPL originates from structural modifications of the external granule layer and has the ability to generate neuronal precursors on the cerebellar surface. Analyses of neurogenesis in the cerebellum at different stages, by the detection of Ki67 and BrdU, revealed marked cell proliferation occurring around puberty (12). In addition, it was notable that a number of newly born cells were detectable in fully adult rabbits (1-2 years old) in the absence of a germinative SPL.…”

“…A previous study described the existence of a secondary germinal matrix persisting after puberty in a subpial position of the cerebellum, called the subpial layer (SPL), in the New Zealand white rabbit (12). The SPL originates from structural modifications of the external granule layer and has the ability to generate neuronal precursors on the cerebellar surface.…”