Fighting Assessment Triggers Rapid Changes in Activity of the Brain Social Decision-Making Network of Cichlid Fish

Abstract

Social living animals have to adjust their behavior to rapid changes in the social environment. It has been hypothesized that the expression of social behavior is better explained by the activity pattern of a diffuse social decision-making network (SDMN) in the brain than by the activity of a single brain region. In this study, we tested the hypothesis that it is the assessment that individuals make of the outcome of the fights, rather than the expression of aggressive behavior per se, that triggers changes in the pattern of activation of the SDMN which are reflected in socially driven behavioral profiles (e.g., dominant vs. subordinate specific behaviors). For this purpose, we manipulated the perception of the outcome of an agonistic interaction in an African cichlid fish (Oreochromis mossambicus) and assessed if either the perception of outcome or fighting by itself was sufficient to trigger rapid changes in the activity of the SDMN. We have used the expression of immediate early genes (c-fos and egr-1) as a proxy to measure the neuronal activity in the brain. Fish fought their own image on a mirror for 15 min after which they were allocated to one of three conditions for the two last minutes of the trial: (1) they remained fighting the mirror image (no outcome treatment); (2) the mirror was lifted and a dominant male that had just won a fight was presented behind a transparent partition (perception of defeat treatment); and (3) the mirror was lifted and a subordinate male that had just lost a fight was presented behind a transparent partition (perception of victory treatment). Results show that these short-term social interactions elicit distinct patterns in the SDMN and that the perception of the outcome was not a necessary condition to trigger a SDMN response as evidenced in the second treatment (perception of defeat treatment). We suggest that the mutual assessment of relative fighting behavior drives these acute changes in the state of the SDMN.

Keywords: androgens; challenge hypothesis; immediate early genes; social competence; social decision making network.

Figure 1

Behavioral paradigm. (A) 3D diagram of the experimental setup. Test tank and demo tank were side-by-side and physically separated. (B) Schematic of the experimental treatments. Focal fish interacted with a mirror for 15 min while two males were fighting in the adjacent compartment. Then, focal fish were allowed to see for 2 min its own image in the mirror (MM treatment), a dominant male (Mirror becomes Dominant—MD treatment) or a subordinate male (Mirror becomes Subordinate—MS treatment).

Figure 2

Variation in the behavioral component scores obtained with the Principal Component Analysis (PCA) for each experimental treatment. (A) PC1 interpreted as “overt aggression”; and (B) PC2 interpreted as “aggressive motivation.” *Significant difference for p < 0.05; **significant difference for p < 0.01. Results are expressed as mean ± standard error of the mean (SEM).

Figure 3

Expression of the immediate early genes (IEG) c-fos and egr-1 in several brain areas of the social decision-making network (SDMN). GC, central gray; PPa, anterior part of the periventricular preoptic nucleus; TA, nucleus anterior tuberis; VVm, medial part of the ventral subdivision of the ventral telencephalon; Vs, supracommissural nucleus of the ventral telencephalon. *Significant difference for p < 0.05. Results are expressed as mean ± standard error of the mean (SEM).

Figure 4

Representation of the state of the SDMN and the behavior for all the experimental treatments. Node size of each brain area indicates the activity level at each network node using c-fos and egr-1 as reporters of neural activity. PC1 and PC2, component loadings obtained with the PCA of aggressive behavior were used as behavioral network nodes, where the node size corresponds to the average of principal component scores within each treatment. Line thickness indicates the strength of the connection between nodes (measured with Pearson correlation coefficients, r-value); green lines represent positive correlations; red lines represent negative correlations. GC, central gray; PPa, anterior part of the periventricular preoptic nucleus; TA, nucleus anterior tuberis; VVm, medial part of the ventral subdivision of the ventral telencephalon; Vs, supracommissural nucleus of the ventral telencephalon. PC1, first component loading interpreted as “overt aggression”; PC2, second component loading interpreted as “aggressive motivation.” **Significant correlations after p-value adjustment for p < 0.01.

Figure 5

Variation in androgen levels and expression of gnrh1 in the Ppa of the focal fish for each experimental condition. (A) 11-Ketotestosterone (KT) levels; (B) Testosterone (T) levels; (C) gnrh1 expression. Results are expressed as mean ± standard error of the mean (SEM).