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Social dominance is prevalent throughout the animal kingdom. It facilitates the stabilization of social relationships and allows animals to divide resources according to social rank. Zebrafish form stable dominance relationships that consist of dominants and subordinates. Although social-status-dependent differences in behavior must arise due to neural plasticity, mechanisms of how neural circuits are reconfigured to cope with social dominance are poorly described. Here, we describe how the posterior tuberculum nucleus (PT), which integrates sensory social information to modulate spinal motor circuits, is morphologically and functionally influenced by social status. We combined non-invasive behavioral monitoring of motor activity (startle escape and swim) and histological approaches to investigate how social dominance affects the morphological structure, axosomatic synaptic connectivity, and functional activity of the PT in relation to changes in motor behavior. We show that dopaminergic cell number significantly increases in dominants compared to subordinates, while PT synaptic interconnectivity, demonstrated with PSD-95 expression, is higher in subordinates compared to dominants. Secondly, these socially induced morphological differences emerge after one week of dominance formation and correlate with differences in cellular activities illustrated with higher phosphor-S6 ribosomal protein expression in dominants compared to subordinates. Thirdly, these morphological differences are reversible as the social environment evolves and correlates with adaptations in startle escape and swim behaviors. Our results provide new insights of the neural bases of social behavior that may be applicable to other social species with similar structural and functional organization. 

Animals exhibit context-dependent behavioral decisions that are mediated by specific motor circuits. In social species these decisions are often influenced by social status. Although social status-dependent neural plasticity of motor circuits has been investigated in vertebrates, little is known of how cellular plasticity translates into differences in motor activity. Here, we used zebrafish (Danio rerio) as a model organism to examine how social dominance influences the activation of swimming and the Mauthner-mediated startle escape behaviors. We show that the status-dependent shift in behavior patterns whereby dominants increase swimming and reduce sensitivity of startle escape while subordinates reduce their swimming and increase startle sensitivity is regulated by the synergistic interactions of dopaminergic, glycinergic, and GABAergic inputs to shift the balance of activation of the underlying motor circuits. This shift is driven by socially induced differences in expression of dopaminergic receptor type 1b (Drd1b) on glycinergic neurons and dopamine (DA) reuptake transporter (DAT). Second, we show that GABAergic input onto glycinergic neurons is strengthened in subordinates compared with dominants. Complementary neurocomputational modeling of the empirical results show that drd1b functions as molecular regulator to facilitate the shift between excitatory and inhibitory pathways. The results illustrate how reconfiguration in network dynamics serves as an adaptive strategy to cope with changes in social environment and are likely conserved and applicable to other social species.