Socially mediated shift in neural circuits activation regulated by synergistic neuromodulatory signaling

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 reuptake transporter (dat). Secondly, we show that GABAergic input onto glycinergic neurons is strengthened in subordinates compared to 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.Significance StatementThe neural mechanisms underlying social behavior remain poorly understood. The study shows how synaptic plasticity of dopaminergic, GABAergic, and glycinergic inputs synergistically modulate zebrafish startle escape and swim behavior in a social status-dependent manner. Socially driven changes in drd1b expression in glycinergic neurons shifts the balance between excitatory (dopaminergic) and inhibitory (glycinergic and GABAergic) pathways highlighting the importance of drd1b as a molecular regulator of adaptive social behavior.