The effect of observers on behavior and the brain during aggressive encounters

Abstract

What effect does an audience have on an animal’s behavior and where is this influence registered in the brain? To answer these questions, we analyzed male cichlid fish fighting in the presence of audiences of various compositions and measured expression of immediate early genes in the brain as a proxy for neural activity. We hypothesized their behavior would change depending on who was watching them. We measured behavioral responses from both the “watchers” and the “watched” during aggressive encounters and found that males fighting in the presence of an audience were more aggressive than males fighting without an audience. Depending on the nature of the audience, immediate early gene expression in key brain nuclei was differentially influenced. Both when an audience of larger males watched fighting males, and when they were watching larger males fighting, nuclei in the brain considered homologous with mammalian nuclei known to be associated with anxiety showed increased activity. When males were in the presence of any audience or when males saw any other males fighting, nuclei in the brain known to be involved in reproduction and aggression were differentially activated relative to control animals. In all cases, there was a close relationship between patterns of brain gene expression between fighters and observers. This suggests that the network of brain regions known as the social behavior network, common across vertebrates, are activated not only in association with the expression of social behavior but also by the reception of social information.

Hippocampal‐like circuitry in the pallium of an electric fish: Possible substrates for recursive pattern separation and completion

“…This is important because extensive studies have shown that the expression of the immediate early gene Egr‐1, which has been linked to long‐term social memory in Apteronotus (Harvey‐Girard et al, 2011), is highly conserved in this species (Burmeister et al, ). Fernald and colleagues have shown that social interactions can induce Egr‐1 expression in various brain regions, including DL and DM (Burmeister et al, ; Maruska et al, ; Desjardins et al, ). These studies were done using microdissected brain regions and did not evaluate Egr‐1 mRNA expression in DC2 (DD?).…”

Cichlids as a Model System for Studying Social Behaviour and Evolution

“…Not only will this vastly expand the number of candidate species, but it will also facilitate studies into patterns of neural activity in response to social stimuli through quantiଏcation of immediate early gene (IEG) expression levels (e.g. transcription factors c-Fos, EGR-1) in candidate regions of the SDMN using similar approaches to numerous neuroethological studies involving ଏshes (Desjardins et al 2015;Maruska et al 2013;Roleira et al 2017;Teles et al 2015Teles et al , 2016Weitekamp and Hofmann 2017). Cichlids are also amenable to CRISPR gene editing and other genetic tools that allow selective manipulation of candidate neural circuits involved in social interactions (Juntti 2019), providing experimental potential to examine candidate mechanistic pathways underlying social behaviour.…”

Audience Effects in Territorial Defense of Male Cichlid Fish Are Associated with Differential Patterns of Activation of the Brain Social Decision-Making Network

“…In a mate choice paradigm, Astatotilapia burtoni females showed a different pattern of activation of SDMN nodes after watching their preferred mate either winning or losing an agonistic interaction: SDMN nodes related to reproduction (i.e., pre-optic area and fish homolog of the ventromedial hypothalamus) were activated when their preferred mate won the fight, whereas nodes linked to anxiety (i.e., fish homolog of the lateral septum) were more active when their preferred mate lost the fight (Desjardins et al, 2010 ). In another study, relative body size has also been shown to influence the pattern of activation of SDMN nuclei, with larger body size inducing a higher activation of brain regions related to anxiety, both in fighting fish perceiving a audience made up of larger fish, or in eavesdroppers attending a fight between larger individuals (Desjardins et al, 2015 ). Finally, in zebrafish the brain transcriptomic changes associated with social eavesdropping have been shown to comprise an up-regulation of genes related to alertness and memory formation in fish eavesdropping a fight between conspecifics (Lopes et al, 2015 ).…”