Experimental evidence for sex-specific plasticity in adult brain

Abstract

BackgroundPlasticity in brain size and the size of different brain regions during early ontogeny is known from many vertebrate taxa, but less is known about plasticity in the brains of adults. In contrast to mammals and birds, most parts of a fish’s brain continue to undergo neurogenesis throughout adulthood, making lifelong plasticity in brain size possible. We tested whether maturing adult three-spined sticklebacks (Gasterosteus aculeatus) reared in a stimulus-poor environment exhibited brain plasticity in response to environmental enrichment, and whether these responses were sex-specific, thus altering the degree of sexual size dimorphism in the brain.ResultsRelative sizes of total brain and bulbus olfactorius showed sex-specific responses to treatment: males developed larger brains but smaller bulbi olfactorii than females in the enriched treatment. Hence, the degree of sexual size dimorphism (SSD) in relative brain size and the relative size of the bulbus olfactorius was found to be environment-dependent. Furthermore, the enriched treatment induced development of smaller tecta optica in both sexes.ConclusionsThese results demonstrate that adult fish can alter the size of their brain (or brain regions) in response to environmental stimuli, and these responses can be sex-specific. Hence, the degree of SSD in brain size can be environment-dependent, and our results hint at the possibility of a large plastic component to SSD in stickleback brains. Apart from contributing to our understanding of the processes shaping and explaining variation in brain size and the size of different brain regions in the wild, the results show that provision of structural complexity in captive environments can influence brain development. Assuming that the observed plasticity influences fish behaviour, these findings may also have relevance for fish stocking, both for economical and conservational purposes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-015-0130-0) contains supplementary material, which is available to authorized users.

Environmental enrichment, sexual dimorphism, and brain size in sticklebacks

“…The same applied to body size, body mass, and condition of the fish, indicating a lack of positive effect on growth and energy balance of the individuals. Although similar outcomes have been recorded in some earlier studies (reviewed in Näslund & Johnsson, 2016), our findings are noteworthy in light of the results from an earlier study conducted on this species, which found evidence for a positive effect of enrichment on male brain size (Herczeg et al., 2015). In contrast, we found that the degree of sexual size dimorphism (SSD) in brain was similar in both treatments and all populations included in the current study.…”

“…To this end, we conducted a common garden experiment in which fish from four different populations were exposed to either a control (bare aquaria) or enriched (spatial complexity generated with physical structures) treatment over a period of 2 months. Based on the results of an earlier experiment which found that males developed larger brains in enriched tanks as compared to females (Herczeg et al., 2015), we expected to see a similar sex‐specific response to environmental enrichment consistent across the four populations tested. Apart from assessing the treatment effects on brain size and size of different brain parts, we also investigated how enrichment influenced growth (i.e., body size) and condition (i.e., residual mass) of the fish.…”

“…Likewise, given the high energetic costs of maintaining neural tissue, the ability to reduce the size of the brain or a particular brain part through phenotypic plasticity when they are not critical for fitness should be favored by selection. It has been proposed that the sexual dimorphism in the three‐spined stickleback brain might be subject to sex‐specific plasticity such that males increase their brain size during the breeding season in response to the increased cognitive demands imposed by mating, nest‐guarding, and parental demands (Herczeg, Gonda, Balazs, Noreikiene, & Merilä, 2015). In this scenario, such plasticity could be adaptive, as the males would escape the energetic costs of maintaining large brains during the nonbreeding season.…”

“…While some studies have supported this finding of positive effects of enrichment on brain size (DePasquale, Neuberger, Hirrlinger, & Braithwaite, 2016; Herczeg et al., 2015; Näslund, Aarestrup, Thomassen, & Johnsson, 2012), others have found either negative effects (Kotrschal, Sundström, Brelin, Devlin, & Kolm, 2012; Turschwell and White, 2016) or none at all (Burns, Saravanan, & Rodd, 2009; Kihslinger, Lema, & Nevitt, 2006). This is true not only for overall brain size, but also in the size of certain brain regions such as the cerebellum, olfactory bulb, telencephalon, and optic tectum in which both positive (Herczeg et al., 2015; Kihslinger & Nevitt, 2006; Kotrschal, Rogell, Maklakov, & Kolm, 2012; Näslund et al., 2012) and negative (optic tectum; Herczeg et al., 2015) effects of environmental enrichment have been shown. However, in the cases where positive effects have been found, the effects have been conditional to age (Näslund et al., 2012), sex, and social interactions (Herczeg et al., 2015; Kotrschal, Rogell et al., 2012) or other factors such as stress (DePasquale et al., 2016).…”

“…This is true not only for overall brain size, but also in the size of certain brain regions such as the cerebellum, olfactory bulb, telencephalon, and optic tectum in which both positive (Herczeg et al., 2015; Kihslinger & Nevitt, 2006; Kotrschal, Rogell, Maklakov, & Kolm, 2012; Näslund et al., 2012) and negative (optic tectum; Herczeg et al., 2015) effects of environmental enrichment have been shown. However, in the cases where positive effects have been found, the effects have been conditional to age (Näslund et al., 2012), sex, and social interactions (Herczeg et al., 2015; Kotrschal, Rogell et al., 2012) or other factors such as stress (DePasquale et al., 2016). Hence, there is a great deal of heterogeneity in the observed responses to environmental enrichment, but there remains little understanding of the causes underlying this heterogeneity.…”