Social Opportunity Causes Rapid Transcriptional Changes in the Social Behaviour Network of the Brain in an African Cichlid Fish

Abstract

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.

Social information changes the brain

“…The SBN comprises six brain nuclei, or nodes (lateral septum, medial extended amygdala/bed nucleus of the stria terminalis, preoptic area, anterior hypothalamus, ventromedial hypothalamus, and midbrain periaqueductal gray/tegmentum) that are reciprocally connected and express high levels of steroid receptors. Originally identified in mammals (32), homologous regions have been found in reptiles (33), fish (34,35), and birds (33), providing a useful framework for analyzing the neural bases of social behaviors (36,37). The expression of steroid receptors in the SBN nuclei suggests that these nodes are also important neural substrates for integration of social behavior with an animal's hormonal state.…”

“…4). Other studies that use IEGs to examine brain activation in response to social information typically reveal differential patterns of expression depending on the social context, such that, for example, male aggression and male sexual behavior can have distinctly different expression patterns across the SBN nodes (32,34). Social ascent in A. burtoni, however, is associated with simultaneous reproductive and aggressive/territorial contexts, producing a combined activation pattern of all of the SBN nuclei.…”

Social descent with territory loss causes rapid behavioral, endocrine, and transcriptional changes in the brain

“…These studies in fishes, the largest and most diverse group of vertebrates, with >30,000 species, provides crucial and needed comparative data to understand the evolution of coping mechanisms in response to social descent. We compare these results of social descent with our previous analyses of social ascent (subordinate to dominant) (Maruska et al, 2013) in which males gain a territory and reproductive opportunities to understand how the brain coordinates the perception of similar highly salient cues of opposite social valence. Dominance hierarchies and frequent changes in relative status position are widespread in the animal kingdom, so our results have important implications for understanding the evolution of neural mechanisms that mediate status transitions across all taxa.…”

Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain

“…Hence, the same genotype must accommodate the expression of multiple social phenotypes, and this should be accomplished, at least partially, by socially driven changes in gene expression in the brain that would lead to distinct transcriptome profiles across the social behavior neural network (aka neurogenomic states) (3,9,10) corresponding to status-specific behavioral states. Previous studies have established this mapping of socially dependent behavioral states onto neurogenomic states (11)(12)(13)(14), and rapid responses to social interactions have also been described (15)(16)(17)(18). However, the specific cue that signals changes in social status and triggers the switch between neurogenomic states has remained elusive.…”