Functional neuroanatomy and neural oscillations during social eavesdropping in male golden hamsters

Abstract

Social eavesdropping is a low-cost learning mechanism by which individuals extract relevant social information from social interactions between conspecifics, thereby gaining subsequent advantages in information gathering and usage. The aim of this study was to take advantage of a new hamster model of social eavesdropping to investigate behavioral consequences and neural activity in male hamsters during social eavesdropping. Bystander hamsters with a defeat experience were exposed to either a fighting interaction, a neutral encounter, or control conditions for 3 days of social eavesdropping. In Experiment 1, bystanders in the fight and neutral groups displayed more information gathering behaviors and less nonsocial behavior than control hamsters. The fight group displayed significant increases in c-Fos-positive neurons in the anterior mid-cingulate cortex (aMCC) and the piriform cortex. A slight but not significant group difference was found in their serum cortisol levels. In vivo local field potential oscillation recordings in Experiment 2 revealed that bystanders in the fight group had more delta oscillations in the aMCC during information gathering across 3-day social eavesdropping than those in the other 2 groups. Experiment 3 confirmed that 20 min of social eavesdropping on Day 1 was sufficient to evoke differential behavioral outcomes, and the behavioral responses became more prominent after 3 days of social eavesdropping. Collectively, our study confirmed that male golden hamsters are capable of social eavesdropping and indicated the involvement of aMCC delta oscillations in social eavesdropping.