Adult neurogenesis in the central nervous system of teleost fish: from stem cells to function and evolution

Abstract

Adult neurogenesis, the generation of functional neurons from adult neural stem cells in the central nervous system (CNS), is widespread, and perhaps universal, among vertebrates. This phenomenon is more pronounced in teleost fish than in any other vertebrate taxon. There are up to 100 neurogenic sites in the adult teleost brain. New cells, including neurons and glia, arise from neural stem cells harbored both in neurogenic niches and outside these niches (such as the ependymal layer and parenchyma in the spinal cord, respectively). At least some, but not all, of the stem cells are of astrocytic identity. Aging appears to lead to stem cell attrition in fish that exhibit determinate body growth but not in those with indeterminate growth. At least in some areas of the CNS, the activity of the neural stem cells results in additive neurogenesis or gliogenesis – tissue growth by net addition of cells. Mathematical and computational modeling has identified three factors to be crucial for sustained tissue growth and correct formation of CNS structures: symmetric stem cell division, cell death and cell drift due to population pressure. It is hypothesized that neurogenesis in the CNS is driven by continued growth of corresponding muscle fibers and sensory receptor cells in the periphery to ensure a constant ratio of peripheral versus central elements. This ‘numerical matching hypothesis’ can explain why neurogenesis has ceased in most parts of the adult CNS during the evolution of mammals, which show determinate growth.

Transit Amplifying Progenitors in the Cerebellum: Similarities to and Differences from Transit Amplifying Cells in Other Brain Regions and between Species

“…In the remainder of this section, we summarize transit amplification/indirect neurogenesis in the CNS of mammals and Drosophila to explain (1) the differences and similarities between these traditional models (embryonic cerebellar cortex, adult subgranular zone [SGZ], and adult ventral SVZ[V-SVZ]) and a novel model in the cerebellum by describing the transit-amplification in the mammalian CNS, and (2) the evolutionary conservation of this transit-amplification system by describing the Drosophila neuroblast. Although transit amplification/adult neurogenesis has been reported in other species, such as birds [ 16 ] and fish [ 17 ], we will not assess these in this review.…”

Decline in Constitutive Proliferative Activity in the Zebrafish Retina with Ageing

“…As development progresses, proliferative and neurogenic activities are gradually lost in most CNS regions, and, in postnatal life, neurogenic activity is restricted to specific regions called neurogenic niches [ 1 , 2 ]. Moreover, the presence of postnatal neurogenic activity in the CNS was also progressively lost during vertebrate evolution (reviewed in [ 3 , 4 , 5 , 6 , 7 , 8 ]). Accordingly, different vertebrate species show different postnatal/adult proliferative and neurogenic rates and different numbers of neurogenic niches in the CNS, which are more abundant in teleost fishes (reviewed in [ 3 , 4 , 5 , 6 , 7 , 8 , 9 ]).…”

“…Moreover, the presence of postnatal neurogenic activity in the CNS was also progressively lost during vertebrate evolution (reviewed in [ 3 , 4 , 5 , 6 , 7 , 8 ]). Accordingly, different vertebrate species show different postnatal/adult proliferative and neurogenic rates and different numbers of neurogenic niches in the CNS, which are more abundant in teleost fishes (reviewed in [ 3 , 4 , 5 , 6 , 7 , 8 , 9 ]). Some postnatal constitutive and/or inducible (e.g., during regeneration) neurogenic niches are found in the retina of vertebrates.…”

Decline in constitutive proliferative activity in the zebrafish retina with ageing

“…As development progresses, proliferative and neurogenic activities are gradually lost in most CNS regions, and in postnatal life, neurogenic activity is restricted to specific regions called neurogenic niches (Doetsch, 2003;Álvarez-Buylla and Lim, 2004). Moreover, the presence of postnatal neurogenic activity in the CNS was also progressively lost during vertebrate evolution (reviewed in Ferretti, 2011;Zupanc and Sîrbulescu, 2011;Than-Trong and Bally-Cuif, 2015;Alunni and Bally-Cuif, 2016;Zupanc, 2021). Accordingly, different vertebrate species show different postnatal/adult proliferative and neurogenic rates and different numbers of neurogenic niches in the CNS, which are more abundant in teleost fishes (reviewed in Ferretti, 2011;Zupanc and Sîrbulescu, 2011;Than-Trong and Bally-Cuif, 2015;Alunni and Bally-Cuif, 2016;Zupanc, 2021).…”

“…Moreover, the presence of postnatal neurogenic activity in the CNS was also progressively lost during vertebrate evolution (reviewed in Ferretti, 2011;Zupanc and Sîrbulescu, 2011;Than-Trong and Bally-Cuif, 2015;Alunni and Bally-Cuif, 2016;Zupanc, 2021). Accordingly, different vertebrate species show different postnatal/adult proliferative and neurogenic rates and different numbers of neurogenic niches in the CNS, which are more abundant in teleost fishes (reviewed in Ferretti, 2011;Zupanc and Sîrbulescu, 2011;Than-Trong and Bally-Cuif, 2015;Alunni and Bally-Cuif, 2016;Zupanc, 2021). Some postnatal neurogenic niches are found in the retina of vertebrates.…”