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- Evolutionarily conserved role of oxytocin in social fear contagion in zebrafishPublication . 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.
- Sex differences in social buffering and social contagion of alarm responses in zebrafishPublication . Akinrinade, Ibukun; Varela, Susana.A.M.; Oliveira, Rui FilipeThe alarm substance in fsh is a pheromone released by injured individuals after a predator attack. When detected by other fsh, it triggers fear/defensive responses, such as freezing and erratic movement behaviours. Such responses can also help other fsh in the shoal to modulate their own behaviours: decreasing a fear response if conspecifcs have not detected the alarm substance (social bufering) or triggering a fear response if conspecifcs detected the alarm substance (social contagion). Response variation to these social phenomena is likely to depend on sex. Because males have higher-risk life-history strategies than females, they may respond more to social bufering where they risk not responding to a real predator attack, while females should respond more to social contagion because they only risk responding to a false alarm. Using zebrafsh, we explored how the response of males and females to the presence/absence of the alarm substance is modifed by the alarmed/ unalarmed behaviour of an adjacent shoal of conspecifcs. We found that, in social bufering, males decreased freezing more than females as expected, but in social contagion males also responded more than females by freezing at a higher intensity. Males were, therefore, more sensitive to visual information, while females responded more to the alarm substance itself. Because visual information updates faster than chemical information, males took more risks but potentially more benefts as well, because a quicker adjustment of a fear response allows to save energy to other activities. These sex diferences provide insight into the modifying efect of life-history strategies on the use of social information.
- Sex differences in aggression are paralleled by differential activation of the brain social decision-making network in ZebrafishPublication . 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.