Animals constantly integrate external stimuli with their own internal physiological state to make appropriate behavioural decisions. Little is known, however, about where in the brain the salience of these signals is evaluated, or which neural and transcriptional mechanisms link this integration to adaptive behaviours. We used an African cichlid fish Astatotilapia burtoni to test the hypothesis that a new social opportunity activates the conserved ‘social behaviour network’ (SBN), a collection of brain nuclei known to regulate social behaviours across vertebrates. We measured mRNA levels of immediate early genes (IEGs) in microdissected brain regions as a proxy for neuronal activation, and discovered that IEGs were higher in all SBN nuclei in males that were given an opportunity to rise in social rank compared to control stable subordinate and dominant individuals. Further, since the presence of sex-steroid receptors is one defining criteria of SBN nuclei, we also tested whether social opportunity or status influenced androgen and oestrogen receptor mRNA levels within these same regions. There were several rapid region-specific changes in receptor mRNA levels induced by social opportunity, most notably in oestrogen receptor subtypes in areas that regulate social aggression and reproduction, suggesting that oestrogenic signalling pathways play an important role in regulating male status. Several receptor mRNA changes occurred in regions with putative homologies to the mammalian septum and extended amygdala, two regions shared by SBN and reward circuits, suggesting an important role in integration of social salience, stressors, hormonal state, and adaptive behaviours. We also show increases in plasma sex- and stress-steroids at 30-min after a rise in social rank. This rapid endocrine and transcriptional response suggests that the SBN is involved in the integration of social inputs with internal hormonal state to facilitate the transition to dominant status, which ultimately leads to improved fitness for the previously reproductively-suppressed individual.

SUMMARYIn social species that form hierarchies where only dominant males reproduce, lower-ranking individuals may challenge higherranking ones, often resulting in changes in relative social status. How does a losing animal respond to loss of status? Here, using the African cichlid fish Astatotilapia burtoni, we manipulated the social environment, causing males to descend in rank, and then examined changes in behavior, circulating steroids and immediate early gene (IEG) expression (cfos, egr-1) in micro-dissected brain regions as a proxy for neuronal activation. In particular, we examined changes in the conserved 'social behavior network' (SBN), a collection of brain nuclei known to regulate social behaviors across vertebrates. Astatotilapia burtoni has rapidly reversible dominant-subordinate male phenotypes, so that within minutes, descending males lost their bright body coloration, switched to submissive behaviors and expressed higher plasma cortisol levels compared with non-descending and control males. Descending males had higher IEG expression throughout the SBN, but each brain region showed a distinct IEG-specific response in either cfos or egr-1 levels, but not both. Overall, SBN IEG patterns in descending males were distinctly different from the pattern observed in males ascending (subordinate to dominant) in social status. These results reveal that the SBN rapidly coordinates the perception of social cues about status that are of opposite valence, and translates them into appropriate phenotypic changes. This shows for the first time in a non-mammalian vertebrate that dropping in social rank rapidly activates specific socially relevant brain nuclei in a pattern that differs from when males rise to a higher status position.