Social Plasticity Relies on Different Neuroplasticity Mechanisms across the Brain Social Decision-Making Network in Zebrafish

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.

Social Plasticity in the Fish Brain: Neuroscientific and Ethological Aspects

“…Similar types of social status differences are also observed in other fish species [e.g. zebrafish, as mentioned above; other cichlids, electric fish, salmonids, and others; (Gilmour et al, 2005;Maruska, 2014;Miller et al, 2017;Perrone and Silva, 2018;Teles et al, 2016)], and in some cases result in a change in an individuals' sex (male to female, or vice versa) that is accompanied by plasticity in neural circuits (Black et al, 2005;Semsar et al, 2001;Todd et al, 2018). These examples support the broad relevance of fish for addressing questions related to how an animal's social rank impacts their brain and reproductive fitness, health, and survival.…”

“…Zebrafish also offer the opportunity to force social interactions and status transitions to discover underlying mechanisms. In one zebrafish study (Teles et al 2016), four social phenotypes were experimentally induced: winners and losers of a identified markers of social plasticity associated with social status changes: winners were characterized by greater expression of neurogenesis genes (wnt3 and neurod) in Dm, and of neuroligin genes in Vv and Vs (see Table 1 for homologies); and losers were characterized by greater expression of bdnf in Dl and of wnt3 in Vv, and by lower expression of nlgn2 in Vs (Teles et al 2016). These results suggest the participation of mechanisms of neural plasticity in the establishment of social hierarchies in zebrafish.…”

“…also established a model for social rank stress in zebrafish, forcing a dyadic interaction for five days -after which dominance was successfully established. After the establishment of dominance, both subordinates and dominant males showed higher whole-trunk cortisol concentrations than control animals; no differences were observed, however, between dominant and subordinate animals Teles et al (2016). showed a significant increase in cortisol in winner animals (that is, animals which win a 30 min fight against a…”

“…The ability to adapt to changing social environments is a crucial characteristic of biological systems; social plasticity, defined "as the ability to adaptively change the expression of social behavior according to previous experience and to social context" (Teles et al 2016) is a key ecological performance trait that should be viewed as crucial discovered by examining a wider variety of social arrangements than relying on a single species. Both issues are discussed in Sections 2 to 4.…”

Region-specific neuron recruitment in the hippocampus of brown-headed cowbirdsMolothrus ater(Passeriformes: Icteridae)

“…For instance, sensory inputs from forebrain sensory regions enter specific Hp sub-regions and send output to regions regulating affective and motivational processes, including the septum and the hypothalamus (Atoji & Wild 2006). In addition, the avian hippocampus has a remarkable capacity for structural reorganization as is the case in other vertebrates, including mammals and fish (Zupanc 2006;Gu et al 2012;Burger et al 2014;Teles et al 2016). However, even some measures of neural reorganization vary along the subdivisions of the avian Hp (Barnea & Nottebohm 1994).…”