Comparative social cognition: zebrafish as a neurobehavioural model

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Publications

Brain transcriptomic response to social eavesdropping in zebrafish (Danio rerio)

Publication . Lopes, Joao Sollari; Abril-de-Abreu, Rodrigo; Oliveira, Rui Filipe

Public information is widely available at low cost to animals living in social groups. For instance, bystanders may eavesdrop on signaling interactions between conspecifics and use it to adapt their subsequent behavior towards the observed individuals. This social eavesdropping ability is expected to require specialized mechanisms such as social attention, which selects social information available for learning. To begin exploring the genetic basis of social eavesdropping, we used a previously established attention paradigm in the lab to study the brain gene expression profile of male zebrafish (Danio rerio) in relation to the attention they paid towards conspecifics involved or not involved in agonistic interactions. Microarray gene chips were used to characterize their brain transcriptomes based on differential expression of single genes and gene sets. These analyses were complemented by promoter regionbased techniques. Using data from both approaches, we further drafted protein interaction networks. Our results suggest that attentiveness towards conspecifics, whether interacting or not, activates pathways linked to neuronal plasticity and memory formation. The network analyses suggested that fos and jun are key players on this response, and that npas4a, nr4a1 and egr4 may also play an important role. Furthermore, specifically observing fighting interactions further triggered pathways associated to a change in the alertness status (dnajb5) and to other genes related to memory formation (btg2, npas4b), which suggests that the acquisition of eavesdropped information about social relationships activates specific processes on top of those already activated just by observing conspecifics.

2015Journal article

Open access

Social dominance modulates eavesdropping in zebrafish

Publication . Abril-de-Abreu, Rodrigo; Cruz, Ana S.; Oliveira, Rui Filipe

Group living animals may eavesdrop on signalling interactions between conspecifics and integrate it with their own past social experience in order to optimize the use of relevant information from others. However, little is known about this interplay between public (eavesdropped) and private social information. To investigate it, we first manipulated the dominance status of bystander zebrafish. Next, we either allowed or prevented bystanders from observing a fight. Finally, we assessed their behaviour towards the winners and losers of the interaction, using a custom-made video-tracking system and directional analysis. We found that only dominant bystanders who had seen the fight revealed a significant increase in directional focus (a measure of attention) towards the losers of the fights. Furthermore, our results indicate that information about the fighters' acquired status was collected from the signalling interaction itself and not from post-interaction status cues, which implies the existence of individual recognition in zebrafish. Thus, we show for the first time that zebrafish, a highly social model organism, eavesdrop on conspecific agonistic interactions and that this process is modulated by the eavesdroppers' dominance status. We suggest that this type of integration of public and private information may be ubiquitous in social learning processes.

2015Journal article

Open access

Social eavesdropping in zebrafish: Tuning of attention to social interactions

Publication . Abril-de-Abreu, Rodrigo; Cruz, José; Oliveira, Rui Filipe

Group living animals may eavesdrop on signalling interactions between conspecifics in order to collect adaptively relevant information obtained from others, without incurring in the costs of firsthand information acquisition. This ability (aka social eavesdropping) is expected to impact Darwinian fitness, and hence predicts the evolution of cognitive processes that enable social animals to use public information available in the environment. These adaptive specializations in cognition may have evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms, such as attention, which select the information that is available for learning. Here we used zebrafish to test if attention in a social species is tuned to the exchange of information between conspecifics. Our results show that zebrafish are more attentive towards interacting (i.e. fighting) than towards non-interacting pairs of conspecifics, with the exposure to fighting not increasing activity or stress levels. Moreover, using video playbacks to manipulate form features of the fighting fish, we show that during the assessment phase of the fight, bystanders’ attention is more driven by form features of the interacting opponents; whereas during the post-resolution phase, it is driven by biological movement features of the dominant fish chasing the subordinate fish.

2015Journal article

Open access

Social competence: an evolutionary approach

Publication . Taborsky, Barbara; Oliveira, Rui Filipe

'Social competence' refers to the ability of an individual to optimise its social behaviour depending on available social information. Although such ability will enhance social interactions and thus raise Darwinian fitness, its evolutionary and ecological significance has been largely ignored. Social competence is based on behavioural flexibility. We propose that the study of social competence requires an integrative approach that aims to understand how the brain translates social information into flexible behavioural responses, how flexibility might be constrained by the developmental history of an individual or by trade-offs with other (ecological) competences, and how social plasticity feeds back on fitness. Finally we propose a hypothesis of how social competence can become a driver of social evolution.

2012Journal article

Open access

Audience effects and aggressive priming in agonistic behaviour of male zebrafish, Danio rerio

Publication . Cruz, Ana S.; Oliveira, Rui Filipe

Animals communicate through the exchange of signals. However, third-party individuals can detect and intercept signals not directly sent to them, a phenomenon known as eavesdropping, and the presence of bystanders can influence the signalling behaviour of interacting conspecifics, a phenomenon named the audience effect. So far, research done on audience effects and eavesdropping has been mainly focused on their function, rather than on their proximate mechanisms. For this reason, we were interested in testing the occurrence of audience effects on male zebrafish, a genetically tractable model organism that is emerging as a major candidate for the study of the neural basis of social behaviour. Here, pairs of males were exposed to a mixed-sex shoal, which was used as an audience, at two different times: (1) during a contest between them, to test for an audience effect and (2) before the contest, to test whether this prior exposure influences subsequent agonistic behaviour (i.e. aggressive priming). We analysed the pairs' aggressive signalling during the contest by measuring variables that characterize both the individuals' behaviour and the interaction, and found that pre-exposure to an audience induced a shorter latency to display, an increase in the time dominants spent chasing subordinates and a shorter time to resolve the agonistic interaction. Also, exposure to the audience during the interaction led to a higher number of interactions in which displays occurred, a higher number of resolved interactions with displays and a decrease in the escalation of aggression for resolved interactions. These results add zebrafish to the literature on the audience effect and, most importantly, open the way for the study of the neural mechanisms involved in the processing of social information in a model organism.

2015Journal article

Restricted access