Sex Differences in Aggression Are Paralleled by Differential Activation of the Brain Social Decision-Making Network in Zebrafish

Abstract

Although aggression is more prevalent in males, females also express aggressive behaviors and in specific ecological contexts females can be more aggressive than males. The aim of this work is to assess sex differences in aggression and to characterize the patterns of neuronal activation of the social-decision making network (SDMN) in response to intra-sexual aggression in both male and female zebrafish. Adult fish were exposed to social interaction with a same-sex opponent and all behavioral displays, latency, and time of resolution were quantified. After conflict resolution, brains were sampled and sex differences on functional connectivity throughout the SDMN were assessed by immunofluorescence of the neuronal activation marker pS6. Results suggest that both sexes share a similar level of motivation for aggression, but female encounters show shorter conflict resolution and a preferential use of antiparallel displays instead of overt aggression, showing a reduction of putative maladaptive effects. Although there are no sex differences in the neuronal activation in any individual brain area from the SDMN, agonistic interactions increased neuronal activity in most brain areas in both sexes. Functional connectivity was assessed using bootstrapped adjacency matrices that capture the co-activation of the SDMN nodes. Male winners increased the overall excitation and showed no changes in inhibition across the SDMN, whereas female winners and both male and female losers showed a decrease in both excitation and inhibition of the SDMN in comparison to non-interacting control fish. Moreover, network centrality analysis revealed both shared hubs, as well as sex-specific hubs, between the sexes for each social condition in the SDMN. In summary, a distinct neural activation pattern associated with social experience during fights was found for each sex, suggesting a sex-specific differential activation of the social brain as a consequence of social experience. Overall, our study adds insights into sex differences in agonistic behavior and on the neuronal architecture of intrasexual aggression in zebrafish.