Proliferation zones in the brain of adult gymnotiform fish: A quantitative mapping study

Abstract

Whereas in mammals postnatal neurogenesis, gliogenesis, and angiogenesis appear to be kept at low rates, in fish the capability for the production of new brain cells during adulthood is very pronounced. Many of the newly generated cells originate from germinal layers that maintain their proliferative activity during adulthood. By employing incorporation of the thymidine analogue 5-bromo-2'-deoxyuridine (BrdU) into mitotic active cells, we have quantitatively mapped such proliferation zones in the brain of adult Apteronotus leptorhynchus (Gymnotiformes, Teleostei). In the telencephalon, diencephalon, mesencephalon, and rhombencephalon, the total number of BrdU-labelled cells was low, making up approximately 25% of all mitotic active cells in the brain. Many of these cells were scattered over wide areas. Otherwise, zones of high proliferative activity were typically located at or near the surface of ventricular, paraventricular, and cisternal systems. Approximately 75% of all BrdU-labelled cells found in the brain of adult Apteronotus leptorhynchus were situated in the cerebellum. Zones displaying proliferative activity were restricted to small areas, such as narrow stripes around the midline of corpus cerebelli and valvula cerebelli, the boundary between corpus and valvula, and a large portion of the area covered by the eminentia granularis medialis. Counts indicate that, on average, 100,000 cells, corresponding to approximately 0.2% of the total population of cells in the brain of adult Apteronotus leptorhynchus, are in S-phase within a period of 2 hours. At least part of these newly generated cells is added to the population of already existing cells. This leads to a permanent growth of the brain with increasing size of the fish, a process that appears to slow down only in individuals of relatively advanced age.

Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis

“…(c) Response of cell proliferation to predators is consistent across all three forebrain regions Adult B. occidentalis showed a spatial distribution of proliferating cells in the telencephalon consistent with the adult telencephalon of other teleost species, including two other gymnotiform electric fish: Gymnotus omarorum [36] and Apteronotus leptorhynchus [37]. Within individuals, the density was highly correlated among the three forebrain regions.…”

Stretching the limits: Stem cells in regeneration science

“…In the intact teleostean brain, the rate of continued cell proliferation, relative to the total number of brain cells, has been estimated to be at least one, if not two, orders of magnitude higher than in the intact mammalian brain (Zupanc and Horschke, 1995;Hinsch and Zupanc, 2007). These new cells originate from pluripotent adult stem cells harbored in dozens of specific proliferation zones within the brain (Hinsch and Zupanc, 2006).…”

“…In the absence of injury, many cell types, such as epithelia and blood cells, turn over rapidly, while others, such as hepatocytes, myofibers, osteocytes, and most neurons, have low turnover rates, or do not turn over at all. In organisms that grow throughout life, such as fish, the total number of cells in various tissues increases continuously (Zupanc and Horschke, 1995), indicating that the number of new cells produced is higher than the number of cells lost. The replacement of cells in the absence of injury is called homeostatic regeneration because it precisely maintains the cell number appropriate for the mass and architecture of a tissue.…”

Cellular response after crush injury in adult zebrafish spinal cord

“…An unusual feature of fish CNS is that they are neurogenic and they may continue to generate new neurons throughout normal life even in mature uninjured spinal cord (Leonard et al, 1978;Anderson and Waxman, 1983;Waxman and Anderson, 1985). Most of the previous studies on adult neurogenesis and neuronal regeneration in brain are based on different teleost species (Zupanc and Horschke, 1995;Zupanc et al, 2005;Zupanc and Zupanc, 2006). Although zebrafish has emerged as a powerful animal model to study regeneration for various reasons, very little attention has been paid to study spinal cord regeneration in this species.…”