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  • Evolutionarily conserved role of oxytocin in social fear contagion in zebrafish
    Publication . Akinrinade, Ibukun; Kareklas, Kyriacos; Teles, Magda C; Reis, Thais K.; Gliksberg, Michael; Petri, Giovanni; Levkowitz, Gil; Oliveira, Rui F.
    Emotional contagion is the most ancestral form of empathy. We tested to what extent the proximate mechanisms of emotional contagion are evolutionarily conserved by assessing the role of oxytocin, known to regulate empathic behaviors in mammals, in social fear contagion in zebrafish. Using oxytocin and oxytocin receptor mutants, we show that oxytocin is both necessary and sufficient for observer zebrafish to imitate the distressed behavior of conspecific demonstrators. The brain regions associated with emotional contagion in zebrafish are homologous to those involved in the same process in rodents (e.g., striatum, lateral septum), receiving direct projections from oxytocinergic neurons located in the pre-optic area. Together, our results support an evolutionary conserved role for oxytocin as a key regulator of basic empathic behaviors across vertebrates. Copyright © 2023 The Authors, some rights reserved.
  • Social and asocial learning in zebrafish are encoded by a shared brain network that is differentially modulated by local activation
    Publication . Pinho, Adriano Bastos; Cunliffe, Vincent; Kareklas, Kyriacos; Petri, Giovanni; Oliveira, Rui F.
    Group living animals use social and asocial cues to predict the presence of reward or punishment in the environment through associative learning. The degree to which social and asocial learning share the same mechanisms is still a matter of debate. We have used a classical conditioning paradigm in zebrafish, in which a social (fish image) or an asocial (circle image) conditioned stimulus (CS) have been paired with an unconditioned stimulus (US=food), and we have used the expression of the immediate early gene c-fos to map the neural circuits associated with each learning type. Our results show that the learning performance is similar to social and asocial CSs. However, the brain regions activated in each learning type are distinct and a community analysis of brain network data reveals segregated functional submodules, which seem to be associated with different cognitive functions involved in the learning tasks. These results suggest that, despite localized differences in brain activity between social and asocial learning, they share a common learning module and social learning also recruits a specific social stimulus integration module. Therefore, our results support the occurrence of a common general-purpose learning module, that is differentially modulated by localized activation in social and asocial learning.
  • Sex differences in aggression are paralleled by differential activation of the brain social decision-making network in Zebrafish
    Publication . Scaia, Maria Florencia; Akinrinade, Ibukun; Petri, Giovanni; Oliveira, Rui F.
    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.