BCOMP - Artigos em revistas internacionais
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- Optimistic and pessimistic cognitive judgement bias modulates the stress response and cancer progression in zebrafishPublication . Espigares, Felipe; Alvarado, M. Victoria; Abad-Tortosa, Diana; Varela, Susana A. M.; Sobral, Daniel; Faísca, Pedro; Paixão, Tiago; Oliveira, RuiCognitive judgement bias in decision-making under ambiguity occurs both in animals and humans, with some individuals interpreting ambiguous stimulus as positive (optimism) and others as negative (pessimism). We hypothesize that judgement bias is a personality trait and that individuals with a pessimistic bias would be more reactive to stressors and therefore more susceptible to stress-related diseases than optimistic ones. Here, we show that zebrafish judgment bias is a consistent behavioral trait over time, and that pessimistic and optimistic fish express phenotype-specific neurogenomic responses to stress. Furthermore, both phenotypes show differential activation of the hypothalamic-pituitary-interrenal axis in response to chronic stress, suggesting that optimists have a lower stress reactivity. Accordingly, optimists seem to be more resilient to disease than pessimists, as shown by a lower tumorigenesis in a zebrafish melanoma line [Tg(mtifa:HRAS-GFP)]. Together these results indicate that judgement bias is paralleled by differences in the stress response with implications for disease resilience.
- 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.
- 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.
- 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.
- 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.
- The polygenic and reactive nature of observed parentingPublication . Runze, Jana; Bakermans-Kranenburg, Marian; Cecil, Charlotte A M; van IJzendoorn, Marinus; Pappa, IreneIn Wertz et al. (2019), parents' polygenic scores of educational attainment (PGS-EA) predicted parental sensitive responses to the child's needs for support, as observed in a dyadic task (i.e., observed sensitivity). We aimed to replicate and expand these findings by combining longitudinal data, child genotype data and several polygenic scores in the Generation R Study. Mother–child dyads participated in two developmental periods, toddlerhood (14 months old; n = 648) and early childhood (3–4 years old, n = 613). Higher maternal PGS-EA scores predicted higher observed sensitivity in toddlerhood (b = 0.12, 95% CI 0.03, 0.20) and early childhood (b = 0.16, 95% CI 0.08, 0.24). Child PGS-EA was significantly associated with maternal sensitivity in early childhood (b = 0.11, 95% CI 0.02, 0.21), and the effect of maternal PGS-EA was no longer significant when correcting for child PGS-EA. A latent factor of PGSs based on educational attainment, intelligence (IQ) and income showed similar results. These polygenic scores might be associated with maternal cognitive and behavioral skills that help shape parenting. Maternal PGSs predicted observed sensitivity over and above the maternal phenotypes, showing an additional role for PGSs in parenting research. In conclusion, we replicated the central finding of Wertz et al. (2019) that parental PGS-EA partially explains parental sensitivity. Our findings may be consistent with evocative gene–environment correlation (rGE), emphasizing the dynamic nature of parenting behavior across time, although further research using family trios is needed to adequately test this hypothesis.
- Pessimistic cognitive bias is associated with enhanced reproductive investment in female zebrafishPublication . Espigares, Felipe; Alvarado, Maria V.; Faísca, Pedro; Abad-Tortosa, Diana; Oliveira, Rui FilipeOptimistic and pessimistic cognitive biases have been described in many animals and are related to the perceived valence of the environment. We, therefore, hypothesize that such cognitive bias can be adaptive depending on environmental conditions. In reward-rich environments, an optimistic bias would be favoured, whereas in harsh environments, a pessimistic one would thrive. Here, we empirically investigated the potential adaptive value of such bias using zebrafish as a model. We first phenotyped female zebrafish in an optimistic/pessimistic axis using a previously validated judgement bias assay. Optimistic and pessimistic females were then exposed to an unpredictable chronic stress protocol for 17 days, after which fish were euthanized and the sectional area of the different ovarian structures was quantified in both undisturbed and stressed groups. Our results show that zebrafish ovarian development responded to chronic stress, and that judgement bias impacted the relative area of the vitellogenic developmental stage, with pessimists showing higher vitellogenic areas as compared with optimists. These results suggest that pessimism maximizes reproductive investment, through increased vitellogenesis, indicating a relationship between cognitive bias and life-history organismal decisions.
- 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.
- Phenotypic architecture of sociality and its associated genetic polymorphisms in zebrafishPublication . Gonçalves, Claúdia; Kareklas, Kyriacos; Teles, Magda C; Varela, Susana.A.M.; Costa, João; Leite, Ricardo B.; Paixão, Tiago; Oliveira, Rui FilipeSociality relies on motivational and cognitive components that may have evolved independently, or may have been linked by phenotypic correlations driven by a shared selective pressure for increased social competence. Furthermore, these components may be domain-specific or of general-domain across social and non-social contexts. Here, we used zebrafish to test if the motivational and cognitive components of social behavior are phenotypically linked and if they are domain specific or of general domain. The behavioral phenotyping of zebrafish in social and equivalent non-social tests shows that the motivational (preference) and cognitive (memory) components of sociality: (1) are independent from each other, hence not supporting the occurrence of a sociality syndrome; and (2) are phenotypically linked to non-social traits, forming two general behavioral modules, suggesting that sociality traits have been co-opted from general-domain motivational and cognitive traits. Moreover, the study of the association between single nucleotide polymorphisms (SNPs) and each behavioral module further supports this view, since several SNPs from a list of candidate “social” genes, are statistically associated with the motivational, but not with the cognitive, behavioral module. Together, these results support the occurrence of general-domain motivational and cognitive behavioral modules in zebrafish, which have been co-opted for the social domain. © 2022 The Authors. Genes, Brain and Behavior published by International Behavioural and Neural Genetics Society and John Wiley & Sons Ltd.