Browsing by Author "Oliveira, Rui F."
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- Autism-associated gene shank3 is necessary for social contagion in zebrafishPublication . Kareklas, Kyriacos; Teles, Magda C; Dreosti, Elena; Oliveira, Rui F.Background Animal models enable targeting autism-associated genes, such as the shank3 gene, to assess their impact on behavioural phenotypes. However, this is often limited to simple behaviours relevant for social interaction. Social contagion is a complex phenotype forming the basis of human empathic behaviour and involves attention to the behaviour of others for recognizing and sharing their emotional or affective state. Thus, it is a form of social communication, which constitutes the most common developmental impairment across autism spectrum disorders (ASD). Methods Here we describe the development of a zebrafish model that identifies the neurocognitive mechanisms by which shank3 mutation drives deficits in social contagion. We used a CRISPR-Cas9 technique to generate mutations to the shank3a gene, a zebrafish paralogue found to present greater orthology and functional conservation relative to the human gene. Mutants were first compared to wild types during a two-phase protocol that involves the observation of two conflicting states, distress and neutral, and the later recall and discrimination of others when no longer presenting such differences. Then, the whole-brain expression of different neuroplasticity markers was compared between genotypes and their contribution to cluster-specific phenotypic variation was assessed. Results The shank3 mutation markedly reduced social contagion via deficits in attention contributing to difficulties in recognising affective states. Also, the mutation changed the expression of neuronal plasticity genes. However, only downregulated neuroligins clustered with shank3a expression under a combined synaptogenesis component that contributed specifically to variation in attention. Limitations While zebrafish are extremely useful in identifying the role of shank3 mutations to composite social behaviour, they are unlikely to represent the full complexity of socio-cognitive and communication deficits presented by human ASD pathology. Moreover, zebrafish cannot represent the scaling up of these deficits to higher-order empathic and prosocial phenotypes seen in humans. Conclusions We demonstrate a causal link between the zebrafish orthologue of an ASD-associated gene and the attentional control of affect recognition and consequent social contagion. This models autistic affect-communication pathology in zebrafish and reveals a genetic attention-deficit mechanism, addressing the ongoing debate for such mechanisms accounting for emotion recognition difficulties in autistic individuals.
- Emotional contagion and prosocial behaviour in fish: An evolutionary and mechanistic approachPublication . Kareklas, Kyriacos; Oliveira, Rui F.In this review, we consider the definitions and experimental approaches to emotional contagion and prosocial behaviour in mammals and explore their evolutionary conceptualisation for studying their occurrence in the evolutionarily divergent vertebrate group of ray-finned fish. We present evidence for a diverse set of fish phenotypes that meet definitional criteria for prosocial behaviour and emotional contagion and discuss conserved mechanisms that may account for some preserved social capacities in fish. Finally, we provide some considerations on how to address the question of interdependency between emotional contagion and prosocial response, highlighting the importance of recognition processes, decision-making systems, and ecological context for providing evolutionary explanations.
- 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.
- Expanding the concept of social behavior to interspecific interactionsPublication . Oliveira, Rui F.; Bshary, RedouanIn pretty much any species, an individual's survival and reproduction depends crucially on the outcome of interactions with other individuals. Key interactions may take place between individuals of the same species but also between individuals belonging to different species. However, the most accepted definition of social behavior only considers interactions between conspecifics. Here, we argue that the distinction between intra- and interspecific interactions is largely artificial and hinders the integration of the historically separately developed concepts. At the ultimate level, given that the ecological landscape of organisms is composed both by interactions with conspecifics and with heterospecifics, and both types of interactions may have evolutionary consequences. Although intraspecific interactions usually have a higher impact in fitness because in most species interactions relevant for reproduction (mating, parenting) exclusively involve conspecifics, and interactions relevant for survival are more probable between conspecifics because they share the same ecological niche, hence competing for the same resources (e.g., food, shelter), there are notable exceptions in both fitness components (e.g., heterospecific mating in parthenogenic all-female species; heterospecific brood parasitism; heterospecific aggression in sympatric species that compete for shared resources). At the proximate level, behaviors and cognitive decision-making rules used to interact with other organisms may be shared between intra- and interspecific interactions, and the mechanistic differences between conspecific social behaviors used in distinct functional domains, such as mating, aggression, or parenting, can be more expressive than those found within the same functional domain between conspecific and heterospecific behavior. Therefore, there are neither fundamental conceptual (ultimate) reasons, nor key differences in mechanisms underlying behaviors involved in conspecific vs. heterospecific interactions that support the exclusion of interspecific interactions from the conceptual framework of social behavior
- Interaction between vasotocin and gonadal hormones in the regulation of reproductive behavior in a cichlid fishPublication . Almeida, Olinda; Félix, Ana Sofia; Oliveira, Rui F.Vasotocin (VT) has been associated with the regulation of diferent aspects of social behavior (e.g., mating and aggression). Given the fact that androgens are also known to regulate reproductive behavior, we hypothesized that VT and androgens could be interacting, rather than acting independently, in the regulation of reproductive behavior. In the present study, we aimed to understand the efect of VT and its interaction with gonadal hormones (putatively androgens) on diferent aspects of reproductive behavior of a polygynous and territorial cichlid fsh, the Mozambique tilapia (Oreochromis mossambicus). Using a within-subject design, we treated territorial males, that were previously castrated or sham-operated, with diferent dosages of VT as well as with a V1A receptor antagonist (Manning compound) and subsequently analyzed their behavior towards females and towards an intruder male. Our results showed that VT afected the behavior of territorial males towards females but not towards males. Specifcally, VT-treated males interacted less with females (i.e., spent less time touching the transparent partition that allowed visual contact with females) and were less aggressive towards females than salinetreated males. Moreover, in sham-operated males, blocking V1A receptors increased the frequency of bites towards females in comparison to saline-treated males, but not in castrated males. This result suggests that VT down-regulates aggressiveness towards females through the action of V1A receptors in the gonads (putatively decreasing androgen secretion), and that androgens up-regulate this behavior. In summary, our results suggest that VT may modulate social behavior, through an interaction with gonadal hormones.
- Oxytocin and social isolation: Nonapeptide regulation of social homeostasisPublication . Kareklas, Kyriacos; Oliveira, Rui F.Social isolation imposes physiological and behavioural effects that can have a severe impact on health, but the underlying mechanisms remain poorly understood. We reason that mechanisms responsible for the motivation to interact with others and the cognitive assessment of social interactions also mediate the effects of the lack of social interactions. This is because social isolation stress depends on the ability to maintain homeostasis against objective changes from sensory deprivation under physical isolation and subjective changes from perceived unmet social needs. Here, we review evidence for the conserved role played by the oxytocin neurosignalling system via its modulation of social decision-making and stress management. We discuss how oxytocin underlies the influence of both objective and subjective changes in social conditions, by featuring prominently in the control of motivational and cognitive functions in conserved brain regions, and eliciting ultimate health outcomes through interactions with other neuroendocrine systems. © The Author(s), under exclusive license to Springer Nature Switzerland AG 2024.
- 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.
- Social and asocial learning in zebrafish are encoded by a shared brain network that is differentially modulated by local activationPublication . 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.