Simulated predator stimuli reduce brain cell proliferation in two electric fish species, Brachyhypopomus gauderio and Apteronotus leptorhynchus

Abstract

The brain structure of many animals is influenced by their predators, but the cellular processes underlying this brain plasticity are not well understood. Previous studies showed that electric fish () naturally exposed to high predator () density and tail injury had reduced brain cell proliferation compared with individuals facing few predators and those with intact tails. However, these field studies described only correlations between predator exposure and cell proliferation. Here, we used a congener and another electric fish to experimentally test the hypothesis that exposure to a predator stimulus and tail injury causes alterations in brain cell proliferation. To simulate predator exposure, we either amputated the tail followed by short-term (1 day) or long-term (17-18 days) recovery or repeatedly chased intact fish with a plastic rod over a 7 day period. We measured cell proliferation (PCNA+ cell density) in the telencephalon and diencephalon, and plasma cortisol, which commonly mediates stress-induced changes in brain cell proliferation. In both species, either tail amputation or simulated predator chase decreased cell proliferation in the telencephalon in a manner resembling the effect of predators in the field. In , cell proliferation decreased drastically in the short term after tail amputation and partially rebounded after long-term recovery. In, tail amputation elevated cortisol levels, but repeated chasing had no effect. In , tail amputation elevated cortisol levels in the short term but not in the long term. Thus, predator stimuli can cause reductions in brain cell proliferation, but the role of cortisol is not clear.

Reduced brain cell proliferation following somatic injury is buffered by social interaction in electric fish, Apteronotus leptorhynchus

“…In this experiment, we investigated the combined effect of social interaction and tail amputation on brain cell proliferation, using previously established protocols that demonstrate the separate positive effect of social interaction (Dunlap et al, 2006(Dunlap et al, , 2013 and the negative effect of tail amputation (Dunlap et al, 2017). Initially, all fish were isolated for 4 d. Then focal fish were divided into three treatment groups: fish that were (a) amputated and remained isolated (n = 7; 3 males and 4 females), (b) amputated and paired with a stimulus fish (n = 10; 5 males and 5 females), or (c) left intact and paired with a stimulus fish (n = 7; 4 males and 3 females).…”

“…We tested whether social interaction enhanced brain cell proliferation following 1 d of recovery, during the period when tail injury has the greatest negative effect on brain cell proliferation (Dunlap et al, 2017). All fish were amputated and were divided into two treatment groups: fish that were (a) paired with a partner before (4 d) amputation as well as 1 d following amputation (n = 6, 3 males and 3 females), or (b) isolated both before and after amputation (n = 7, 4 males and 3 females).…”

“…To simulate predator-induced injury, we experimentally amputated the tails of A. leptorhynchus using a procedure identical to that reported previously (Dunlap et al, 2017). To approximate a naturally occurring injury, we cut the tails to remove the caudal 20% of the total body length, which mimics the mean degree of tail loss in another electric fish, B. occidentalis, collected from natural populations (Dunlap et al, 2016;Tran, 2014).…”

“…To measure brain cell proliferation, we used an immunohistochemical procedure similar to that reported earlier (Dunlap et al, 2017). At the conclusion of each experiment, fish were sacrificed by anesthesia (0.075% 2-phenoxyethanol).…”

“…Specifically, in natural populations of Brachyhypopomus occidentalis, in which up to 45% of individuals have tail injuries from predators, field studies showed that tail injury is negatively correlated with forebrain cell proliferation (Dunlap, Tran, Ragazzi, Krahe, & Salazar, 2016). Subsequent laboratory experiments on Brachyhypopomus gauderio and Apteronotus leptorhynchus housed in isolation demonstrated that tail injury indeed causes reduced cell proliferation (Dunlap, Keane, Ragazzi, Lasky, & Salazar, 2017). Fish with experimental tail amputation followed by 7 d recovery produce cells in the forebrain at about half the rate as intact fish.…”