Investigation of behavioral consequence and functional neural activity during social eavesdropping - using male Syrian hamsters as a model

Social eavesdropping is a specific type of social learning. It is defined as extracting information about the relative content of signalers from the interactions between the signalers. Social eavesdropping has advantage in information gathering and has attracted increasing attention. Though many studies have investigated behavioral and developmental consequences of social eavesdropping in animals, the underlying neural mechanisms remain much unclear. Taking advantage of the established social eavesdropping model in Syrian hamsters, we investigated the neural activity of the brain underlying social eavesdropping in hamsters with a single defeated experience. There are three experiments in this study. Adult male Syrian hamsters were randomly assigned into the following three groups: the fight group (subjects exposed to two fighting male hamsters), the neutral group (subjects exposed to an indirect social interaction in which one hamster was constrained in a metal basket), or the non-social control group (an empty arena in Experiment 1 and 3, or social stimuli control group). In Experiment 1, immunochemistry was adopted to map neuronal activities in the selected brains, including piriform cortex, cingulate cortex, hippocampus, and amygdala. We found that males in the fight group had more c-Fos labeled neurons in the anterior mid-cingulate cortex (aMCC) compared with males in the other two groups. Based on the findings in Experiment 1, local field potential was recorded in the aMCC of behaving hamsters to reveal neural activity patterns during social eavesdropping in Experiment 2. The non-social control group was the social stimuli control group in which two demonstrators had no physical and visual contacts with each other. Compared with the social stimuli control group, power spectral density analysis revealed that delta oscillation was increased in the fight group and the neutral group when subjects eavesdropped on the interactions of the demonstrators across the three-day social learning. When there were no demonstrators or social interaction, no difference in the patterns of neural activity was found. Based on the result of Experiment 2, we further investigated the behavioral consequences of one-time and three-time social eavesdropping. Our result demonstrated that 1-day social eavesdropping was sufficient to induce behavioral changes in the bystander even though the learning effect is more pronounced for 3-day social eavesdropping. Collectively, our data suggest that the aMCC might play an important role in social signal detection. This study provides further details regarding social eavesdropping and its neural activity, which may also shed lights on understanding neural mechanisms of social learning.