Abstract
Social living animals need to adjust the expression of their behavior to their status within the group and to changes in social context and this ability (social plasticity) has an impact on their Darwinian fitness. At the proximate level social plasticity must rely on neuroplasticity in the brain social decision-making network (SDMN) that underlies the expression of social behavior, such that the same neural circuit may underlie the expression of different behaviors depending on social context. Here we tested this hypothesis in zebrafish by characterizing the gene expression response in the SDMN to changes in social status of a set of genes involved in different types of neural plasticity: bdnf, involved in changes in synaptic strength; npas4, involved in contextual learning and dependent establishment of GABAergic synapses; neuroligins (nlgn1 and nlgn2) as synaptogenesis markers; and genes involved in adult neurogenesis (wnt3 and neurod). Four social phenotypes were experimentally induced: Winners and Losers of a real-opponent interaction; Mirror-fighters, that fight their own image in a mirror and thus do not experience a change in social status despite the expression of aggressive behavior; and non-interacting fish, which were used as a reference group. Our results show that each social phenotype (i.e., Winners, Losers, and Mirror-fighters) present specific patterns of gene expression across the SDMN, and that different neuroplasticity genes are differentially expressed in different nodes of the network (e.g., BDNF in the dorsolateral telencephalon, which is a putative teleost homolog of the mammalian hippocampus). Winners expressed unique patterns of gene co-expression across the SDMN, whereas in Losers and Mirror-fighters the co-expression patterns were similar in the dorsal regions of the telencephalon and in the supracommissural nucleus of the ventral telencephalic area, but differents in the remaining regions of the ventral telencephalon. These results indicate that social plasticity relies on multiple neuroplasticity mechanisms across the SDMN, and that there is not a single neuromolecular module underlying this type of behavioral flexibility.
Highlights
Social plasticity, defined as the ability to adaptively change the expression of social behavior according to previous experience and to social context, is ubiquitous among group-living animals
The latency for the first bite was significantly lower in mirror-fighters (t = 4.15, df = 20, p < 0.001; Figure 1A), FIGURE 1 | Behavioral characterization of the different social phenotypes. (A) Latency for the first bite; (B) Fight resolution time, the time required for the fight to be solved; (C) the frequency of aggressive and submissive behaviors expressed at the end of the agonistic interactions; error bars represent the standard error of the mean
The results of this study can be interpreted at two different levels: (1) the comparisons between each social treatment (i.e., Winners, Losers, and Mirror-fighters) and the reference group allow the characterization of the neuromolecular response specific to each social treatment; (2) the comparisons of the different social treatments among themselves allow the interpretation of the source of the observed neuromolecular responses, according to the predictions presented at the end of the Introduction
Summary
Social plasticity (aka “social competence,” Taborsky and Oliveira, 2012), defined as the ability to adaptively change the expression of social behavior according to previous experience and to social context, is ubiquitous among group-living animals. The effect of social context on social behavior can be illustrated by different social phenomena present in many different species, such as “dear enemy”/“nasty neighbors” effects (Temeles, 1994; Müller and Manser, 2007), audience effects (Doutrelant et al, 2001; Pinto et al, 2011), social eavesdropping (Oliveira et al, 1998; Earley, 2010), and mate choice copying (Witte and Ryan, 2002) All these examples illustrate how social plasticity allows animals to optimize their social relationships in relation to the complexities of their social environment, and it should be seen as a key determinant of their Darwinian fitness (Oliveira, 2009; Taborsky and Oliveira, 2012). The study of the neuromolecular mechanisms of social plasticity should be seen as a central topic in current behavioral research
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