Environmental complexity, seasonality and brain cell proliferation in a weakly electric fish, Brachyhypopomus gauderio

Abstract

SUMMARYEnvironmental complexity and season both influence brain cell proliferation in adult vertebrates, but their relative importance and interaction have not been directly assessed. We examined brain cell proliferation during both the breeding and non-breeding seasons in adult male electric fish, Brachyhypopomus gauderio, exposed to three environments that differed in complexity: (1) a complex natural habitat in northern Uruguay, (2) an enriched captive environment where fish were housed socially and (3) a simple laboratory setting where fish were isolated. We injected fish with BrdU 2.5h before sacrifice to label newborn cells. We examined the hindbrain and midbrain and quantified the density of BrdU+ cells in whole transverse sections, proliferative zones and two brain nuclei in the electrocommunication circuitry (the pacemaker nucleus and the electrosensory lateral line lobe). Season had the largest effect on cell proliferation, with fish during the breeding season having three to seven times more BrdU+ cells than those during the non-breeding season. Although the effect was smaller, fish from a natural environment had greater rates of cell proliferation than fish in social or isolated captive environments. For most brain regions, fish in social and isolated captive environments had equivalent levels of cell proliferation. However, for brain regions in the electrocommunication circuitry, group-housed fish had more cell proliferation than isolated fish, but only during the breeding season (season ϫ environment interaction). The regionally and seasonally specific effect of social environment on cell proliferation suggests that addition of new cells to these nuclei may contribute to seasonal changes in electrocommunication behavior.

Socially Modulated Cell Proliferation Is Independent of Gonadal Steroid Hormones in the Brain of the Adult Green Treefrog <i>(Hyla cinerea)</i>

“…However, the behavioral response of calling was not driving the socially induced increases in BrdU-labeling in the POA, as demonstrated statistically by controlling for the amount of evoked calling behavior. Thus, unlike that observed in the song control nuclei of songbirds [Wang et al, 1999;Sartor and Ball, 2005] and potentially in the electrocommunication circuitry of electric fish [Dunlap et al, 2006[Dunlap et al, , 2008[Dunlap et al, , 2011, the behavioral output of male treefrogs in this study did not influence cell proliferation in the brain regions studied here.…”

“…Neurogenesis consists of several processes including cell proliferation, differentiation, migration, and survival. These processes have been shown to be modulated by the reception of social stimuli in specialized nuclei related to signal produc-171 tion in mammals [Smith et al, 2001;Fowler et al, 2002;Baudoin et al, 2005], birds [Lipkind et al, 2002;Barnea et al, 2006], fish [Dunlap et al, 2006[Dunlap et al, , 2008[Dunlap et al, , 2011, and crustaceans [Song et al, 2007].…”

Seasonal Variation in Cell Proliferation and Cell Migration in the Brain of Adult Red-Sided Garter Snakes <b><i>(Thamnophis sirtalis parietalis)</i></b>

“…In contrast, social modulation of cell proliferation in the brain of green treefrogs (H. cinerea) is independent of sex steroid hormone concentrations in both males and females, and sex steroids do not directly influence cell proliferation alone [Almli and Wilczynski, 2012]. Similar findings that sex steroid hormones are not the primary factor regulating cell proliferation in the brain have been reported in canaries ( Serinus canaria) [Brown et al, 1993] and weakly electric fish ( Brachyhypopomus gauderio ) [Dunlap et al 2011]. Thus, we speculate that seasonal changes in neurogenesis in redsided garter snakes are probably not regulated by seasonal rhythms in sex steroid hormones, although a regulatory role of glucocorticoid 'stress hormones' is highly likely, particularly as it relates to seasonal changes in allostatic load [e.g.…”

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

“…In many vertebrate taxa, animals in natural populations add brain cells at greater rates than those living in captivity [2,[4][5][6]. One motivation of our study was to address whether the presence of predators, an important feature of most natural habitats, constitutes an environmental enrichment that contributes positively to greater brain cell proliferation in the wild or an environmental stressor that negatively affects brain cell production.…”