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- Brain morphology predicts social intelligence in wild cleaner fishPublication . Triki, Zegni; Emery, Yasmin; Teles, Magda C; Oliveira, Rui Filipe; Bshary, RedouanIt is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence. While these insights are based on many evolutionary studies, it remains unclear how ecology impacts brain plasticity and subsequently cognitive performance within a species. Here, we show that in wild cleaner fish (Labroides dimidiatus), forebrain size of high-performing individuals tested in an ephemeral reward task covaried positively with cleaner density, while cerebellum size covaried negatively with cleaner density. This unexpected relationship may be explained if we consider that performance in this task reflects the decision rules that individuals use in nature rather than learning abilities: cleaners with relatively larger forebrains used decision-rules that appeared to be locally optimal. Thus, social competence seems to be a suitable proxy of intelligence to understand individual differences under natural conditions.
- Social phenotypes in ZebrafishPublication . Nunes, Ana Rita; Ruhl, Nathan; Winberg, Svante; Oliveira, Rui FilipeZebrafish are an established model organism in developmental and behavioral neuroscience, also recently emerging as an excellent model to study social behavior. Zebrafish are highly social, forming groups (shoals) with structured social relationships, dominance hierarchies and overt territoriality. Moreover, social behavior in zebrafish exhibits considerable plasticity both within- (i.e., as a context-dependent behavior) and between individuals (e.g., sex-differences, personality and coping styles) of the same strain, as well as between strains. This richness and plasticity of social behavior, together with the genetic tools available to visualize and manipulate neural circuits in zebrafish places it in the forefront of studying the neurobiological mechanisms underlying complex social behavior. Here, we review the cognitive abilities involved in social behavior, as well as the different functional classes of social behavior present in zebrafish and their variation. We also highlight recent ground-breaking methodological developments in the field, including automated image-based tracking and classification of behavior coupled with video-animated social stimuli, which collectively foster the development of future high-throughput screens of zebrafish social phenotypes.
- 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.
- Immune activation is inversely related to, but does not cause variation in androgen levels in a cichlid fish speciesPublication . Ros, Albert; Oliveira, Rui Filipe; Dijkstra, Peter D.; Groothuis, Ton G.G.Studies on birds and mammals indicate that sexual traits may signal superior health because active immunity, like inflammatory responses to infections, is suppressive to the production of androgens that facilitate the expression of these traits. Here we test this possible pathway for honest signaling in a teleost species, Sarotherodon galilaeus, by activating the immune system with sheep red blood cells (SRBC), which is a non-pathogenic T- and B-cell stimulating antigen. Two weeks after the start of treatment adult males injected with SRBC showed a significant increase in antibody production in comparison with control males. The variation in specific antibody production was negatively related with variation in both testosterone and 11-ketotestosterone levels. This suggests that investment in immune protection is incompatible with increased activity of the hypothalamic-pituitary-gonadal axis. However, opposite to our expectation no difference in androgen levels was found between placebo and SRBC treatment suggesting that immune activation did not cause androgen suppression in our studied species.
- Social zebrafish: Danio rerio as an emerging model in social neuroendocrinologyPublication . Kareklas, Kyriacos; Teles, Magda C; Nunes, Ana Rita; F. Oliveira, RuiThe fitness benefits of social life depend on the ability of animals to affiliate with others and form groups, on dominance hierarchies within groups that determine resource distribution, and on cognitive capacities for recognition, learning and information transfer. The evolution of these phenotypes is coupled with that of neuroendocrine mechanisms, but the causal link between the two remains underexplored. Growing evidence from our research group and others demonstrates that the tools available in zebrafish, Danio rerio, can markedly facilitate progress in this field. Here, we review this evidence and provide a synthesis of the state-of-the-art in this model system. We discuss the involvement of generalized motivation and cognitive components, neuroplasticity and functional connectivity across social decision-making brain areas, and how these are modulated chiefly by the oxytocin-vasopressin neuroendocrine system, but also by reward-pathway monoamine signaling and the effects of sex-hormones and stress physiology.
- Unexpected appetitive events promote positive affective state in juvenile European sea bassPublication . Alvarado, M. V.; Felip, A.; Espigares, F.; Oliveira, Rui FilipeSome animal species exhibit considerable physiological and behavioural alterations in response to captivity. It has been hypothesized, but rarely tested, that such changes reflect a negative affective state that is associated to this specific context. In the last years, judgement bias measures have emerged as reliable indicators of animal affective state, under the assumption that individuals in a negative affective state are more likely to evaluate ambiguous stimuli as negative and display therefore pessimistic behaviours. Here, we have developed a judgement bias task for juvenile European sea bass (Dicentrarchus labrax) aiming to measure optimism/pessimism in this marine species, which have previously been reported to show important dysregulations in captive settings. Our results show that juvenile sea bass exhibit a considerable bias towards pessimistic behaviours in laboratory settings. Furthermore, juveniles that received an unexpected positive event during the judgement bias test displayed more optimistic responses toward ambiguous stimuli as compared to control fish, indicating a positive change in their affective state induced by the appetitive experience. These results reveal a direct interaction of the internal affective state with decision-making processing under ambiguity in juvenile European sea bass, highlighting therefore the potential of judgement bias tests as a tool for the advancement and improvement of our understanding of welfare in finfish aquaculture.
- 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.
- 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.
- 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.
- Innate chemical, but not visual, threat cues have been co‐opted as unconditioned stimulus for social fear learning in zebrafishPublication . Pinho, Julia S.; Castilho, Marisa; Sollari, Joao S.; Oliveira, Rui FilipeAnimals can use social information to detect threat in the environment. In particular, social learning allows animals to learn about dangers without incurring in the costs of trial-and-error learning. In zebrafish, both chemical and visual social cues elicit an innate alarm response, which consists of erratic movement followed by freezing behavior. Injured zebrafish release an alarm substance from their skin that elicits the alarm response. Similarly, the sight of conspecifics displaying the alarm response can also elicit the expression of this response in observers. In this study, we investigated if these social cues of danger can also be used by zebrafish as unconditioned stimulus (US) in learning. We found that only the chemical cue was effective in the social fear conditioning. We suggest that this differential efficacy of social cues results from the fact that the alarm cue is a more reliable indicator of threat, than the sight of an alarmed conspecific. Therefore, although multiple social cues may elicit innate responses not all have been evolutionarily co-opted to act as US in associative learning. Furthermore, the use of the expression of the immediate early genes as markers of neuronal activity showed that chemical social fear conditioning is paralleled by a differential activation of the olfactory bulbs and by a different pattern of functional connectivity across brain regions involved in olfactory processing.
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