Migration of neuronal precursors from the telencephalic ventricular zone into the olfactory bulb in adult zebrafish

Abstract

In the brain of adult mammals, neuronal precursors are generated in the subventricular zone in the lateral wall of the lateral ventricles and migrate into the olfactory bulbs (OBs) through a well-studied route called the rostral migratory stream (RMS). Recent studies have revealed that a comparable neural stem cell niche is widely conserved at the ventricular wall of adult vertebrates. However, little is known about the migration route of neuronal precursors in nonmammalian adult brains. Here, we show that, in the adult zebrafish, a cluster of neuronal precursors generated in the telencephalic ventricular zone migrates into the OB via a route equivalent to the mammalian RMS. Unlike the mammalian RMS, these neuronal precursors are not surrounded by glial tubes, although radial glial cells with a single cilium lined the telencephalic ventricular wall, much as in embryonic and neonatal mammals. To observe the migrating neuronal precursors in living brain tissue, we established a brain hemisphere culture using a zebrafish line carrying a GFP transgene driven by the neurogenin1 (ngn1) promoter. In these fish, GFP was observed in the neuronal precursors migrating in the RMS, some of which were aligned with blood vessels. Numerous ngn1:gfp-positive cells were observed migrating tangentially in the RMS-like route medial to the OB. Taken together, our results suggest that the RMS in the adult zebrafish telencephalon is a functional migratory pathway. This is the first evidence for the tangential migration of neuronal precursors in a nonmammalian adult telencephalon.

Multilineage Differentiation Potential of CNS Cell Progenitors in a Recent Developed Gilthead Seabream (Sparus aurata L.) Nervous Model

“…This behavior is in accordance with the findings of Zupanc et al [50,51] that observed, in the adult fish, RDGc actively divided to produce new neurons in the injured brain and guided them to the lesion site to regenerate the neural tissue [50,51]. Such evidences were supportive for the role exerted by RDGc in adult teleost brain to be responsible for the strong ability of neural tissue regeneration [52]. The possibility that RDGc might exist as radially oriented cells is absolutely dissimilar in mammals, where RDGc were transformed into multipolar astrocytes in the adult brain, no longer regenerating [52,53].…”

“…Such evidences were supportive for the role exerted by RDGc in adult teleost brain to be responsible for the strong ability of neural tissue regeneration [52]. The possibility that RDGc might exist as radially oriented cells is absolutely dissimilar in mammals, where RDGc were transformed into multipolar astrocytes in the adult brain, no longer regenerating [52,53].…”

Mechanisms of Neurogenesis in the Normal and Injured Adult Brain

“…A comparable neural stem cell niche in the adult brain is widely conserved at the ventricular wall 1,[111][112][113][114][115] (Fig. 6), where embryonic neural stem cells are located in the developing brain.…”

“…6). 112 Moreover, a continuous migratory stream of PSA-NCAM+ neuronal progenitors extends from the VZ to the OB, but the neurons do not move through glial tunnels. Time-lapse imaging using Tg(ngn1:gfp) fish demonstrated that neuronal progenitors migrate rostrally along blood vessels in the RMS toward the OB, indicating that the PSA-NCAM+ stream is the functional route for the migration of neuronal progenitors in the adult zebrafish brain.…”

Vasculature-guided neural migration in mouse cerebellum

“…A recent study indicates that neuronal precursors might also use blood vessels as a physical substrate for their migration (Saghatelyan 2009). The vasculature-guided (vasophilic) migration of neuronal precursors has been observed not only under normal conditions, such as in the olfactory bulb (OB) (Bovetti et al 2007;Kishimoto et al 2011;Bozoyan et al 2012), but also in brains undergoing pathological conditions, such as strokes (Saghatelyan 2009). The mechanism of the correlation between nerves and vasculature is not yet clear.…”