Abstract

Modelling complex social behavior in the laboratory is challenging and requires analyses of dyadic interactions occurring over time in a physically and socially complex environment. In the current study, we approached the analyses of complex social interactions in group-housed male CD1 mice living in a large vivarium. Intensive observations of social interactions during a 3-week period indicated that male mice form a highly linear and steep dominance hierarchy that is maintained by fighting and chasing behaviors. Individual animals were classified as dominant, sub-dominant or subordinate according to their David’s Scores and I& SI ranking. Using a novel dynamic temporal Glicko rating method, we ascertained that the dominance hierarchy was stable across time. Using social network analyses, we characterized the behavior of individuals within 66 unique relationships in the social group. We identified two individual network metrics, Kleinberg’s Hub Centrality and Bonacich’s Power Centrality, as accurate predictors of individual dominance and power. Comparing across behaviors, we establish that agonistic, grooming and sniffing social networks possess their own distinctive characteristics in terms of density, average path length, reciprocity out-degree centralization and out-closeness centralization. Though grooming ties between individuals were largely independent of other social networks, sniffing relationships were highly predictive of the directionality of agonistic relationships. Individual variation in dominance status was associated with brain gene expression, with more dominant individuals having higher levels of corticotropin releasing factor mRNA in the medial and central nuclei of the amygdala and the medial preoptic area of the hypothalamus, as well as higher levels of hippocampal glucocorticoid receptor and brain-derived neurotrophic factor mRNA. This study demonstrates the potential and significance of combining complex social housing and intensive behavioral characterization of group-living animals with the utilization of novel statistical methods to further our understanding of the neurobiological basis of social behavior at the individual, relationship and group levels.

Highlights

  • Study of social behavior in laboratory mice has primarily focused on short-term social encounters between familiar or unfamilar dyads [1,2]

  • We show that by acquiring longitudinal observational data on a group of laboratory mice living in a large, complex environment, that it is possible to acquire a detailed understanding of the social behavior of individuals, the temporal patterning of dyadic social relationships and doi:10.1371/journal.pone.0134509.g005

  • We suggest that our findings may support a hypothesis that those individuals with higher corticotrophin releasing factor (CRF) expression in the amygdala (MeA and central amygdala (CeA)) as well as the medial preoptic area of the hypothalamus (mPOA) achieve higher dominance rank through CRF’s actions, elevating levels of aggression and improving the abilities of mice to detect and remember social chemosensory information such that they are more likely to exhibit appropriate subordinate or dominant behavior towards other individuals

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Summary

Introduction

Study of social behavior in laboratory mice has primarily focused on short-term social encounters between familiar or unfamilar dyads [1,2]. The spatial organization of small groups of mice in large arenas has been explored using automated tracking technologies [11,12,13,14] These approaches have low resolution when distinguishing between highly similar behaviors that may occur rapidly or briefly (e.g. fighting, chasing), as well as those behaviors that occur between individuals whose identity may be obscured by other individuals or objects (e.g. nestboxes). These approaches may have significant limitations when used to describe complex social encounters in group-living environments

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