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

Abstract

Environmental 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 × 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.

Fig. 1.

Seasonal variation in brain cell proliferation in the eminentia granularis pars medialis, the major proliferative zone of the hindbrain, of adult Brachyhypopomus gauderio. (A) Breeding season; (B) non-breeding season. The cavity in the lower right of each photograph is the cerebromedullary cistern. Scale bar, 100 μm.

Fig. 2.

BrdU labeling in the brain of adult Brachyhypopomus gauderio. In all photographs, dorsal is towards the top of the figure. (A) Periventricular zone of the anterior midbrain. The cavity at the center is the ventricle. Scale bar, 100 μm. (B) Pacemaker nucleus. Arrows point to BrdU+ cells. The large cells are relay cells, which only show background labeling. Scale bar, 50 μm. (C) Electrosensory lateral line lobe (ELL). Figure shows one lateral half of the ELL, with lateral toward the left. Scale bar, 50 μm.

Fig. 3.

Effect of season on cell proliferation in different brain regions of field active Brachyhypopomus gauderio. The anterior midbrain comprises sections 17–19 and the posterior midbrain comprises sections 14–16, according the Maler brain atlas (Maler et al., 1991). EGm, eminentia granularis pars medialis; ELL, electrosensory lateral line lobe; Pn, pacemaker; PVZ, periventricular zone. Whole section is the density of BrdU+ cells in the whole transverse section. Background is the density of BrdU+ cells in the transverse section outside of proliferative zones (PVZ and EGm). Cell proliferation was significantly higher (P<0.0001) during the breeding season than during the non-breeding season in all brain regions. N=6–8 fish per sample.

Fig. 4.

Effect of environmental complexity on cell proliferation in whole brain, background regions and proliferation zones [eminentia granularis pars medialis (EGm) and periventricular zone (PVZ)] of Brachyhypopomus gauderio. Data are presented only from the breeding season. Note the difference in y-axis scale. *, significant difference from both isolated and group fish; **, significant difference from isolated fish and field fish. N=6–8 fish per sample.

Fig. 5.

Season × environment interactive effect on brain cell proliferation in brain regions of Brachyhypopomus gauderio associated with electrogenesis and electrosensation. Note the difference in y-axis scale. The pacemaker nucleus (Pn) initiates the production of the electric organ discharge, the electrosensory lateral line lobe (ELL) is the primary electrosensory processing region and the anterior midbrain periventricular zone (PVZ) likely contributes cells to the prepacemaker nucleus, which regulates the production of social electric signals. *, significant difference from both isolated and group fish; **, significant different from isolated fish and field fish. N=6–8 fish per sample.

Fig. 6.

Plasma 11-ketotesterone (11kT) levels in Brachyhypopomus gauderio according to season and environment. *, significant difference from both isolated and group fish; **, significant different from isolated fish and field fish. N=5–6 fish per sample.