Advances in understanding neural mechanisms of social dominance

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Dominance hierarchy profoundly impacts social animals’ survival, physical and mental health and reproductive success. As the measurements of dominance hierarchy in rodents become established, it is now possible to understand the neural mechanism mediating the intrinsic and extrinsic factors determining social hierarchy. This review summarizes the latest advances in assay development for measuring dominance hierarchy in laboratory mice. It also reviews our current understandings on how activity and plasticity of specific neural circuits shape the dominance trait and mediate the ‘winner effect’.

Introduction

Social dominance is a universal phenomenon among social animals, ranging from insects [1], fish [2], to rodents [3] and primates [4]. Dominant individuals win more frequently in social competitions. Dominance status strongly impacts an animal's survival, physical and mental health and reproductive success [4, 5, 6]. A lack of motivation to compete in social contests may prevent individuals from realizing their potential. Therefore, understanding the central neural mechanism determining social hierarchy status is of critical importance.

Both intrinsic (physical and mental factors that are inherent and located within, for example, body size/strength, courage/fear, grit/persistency, stress level) and extrinsic factors (factors that are not inherent, acting from the outside, for example, environment, state of ally and opponents, experience such as history of winning/losing) contribute to social status determination. To understand the neural mechanisms underlying these intrinsic and extrinsic factors, simple and robust measurements for social dominance hierarchy are essential. In this review, we summarize the latest advances in the development of social dominance assays. We will also discuss the neuroendocrine regulation and circuit-specific neural activity as two examples of intrinsic factors, and the history of winning/losing as an example of extrinsic factor, and review the major findings in understanding how those factors determine social dominance status.

Section snippets

Tube test

The tube test was developed in 1961 to measure dominance tendency between different mouse strains [7]. For a long time, it was used as a standard assay to screen the behavioral phenotypes of genetically modified mouse lines [8]. Wang et al. established in C57Bl/6 inbred cagemate mice that dominance ranks derived from the tube test are highly linear, stable, and correlate well with ranks derived from several other measures that reflect dominance hierarchy, including barbering, courtship

Neuroendocrine mechanism

To understand the factors contributing to internal traits, early studies were centered around hormonal effects and identified that the level of androgens, especially testosterone, plays a correlative or even causal role in shaping the dominance trait [16, 17, 18, 19, 20]. Testosterone levels rise rapidly (within 45 min) [21] in species ranging from rodents to humans after social competition, generally more in winners than in losers [22]. After testosterone injection, low-ranked hens increased

Neural mechanism mediating the external regulation of social dominance  the ‘winner effect’

Among the external factors that can regulate social dominance, prior history of winning or losing can influence an animal's self-assessment and is an important parameter for the cost-benefit computation in a social competition. The ‘winner/loser effect’, by which winners or losers in previous competitions are more likely to keep winning or losing in future contests [64], exists across a wide range of animal taxa, ranging from insects [65, 66•], crayfish [67], fish [68], birds [69] to humans [70

Concluding remarks and future directions

It is an exciting time to be studying the neural mechanisms of social hierarchy. The field is emerging and many key issues remain to be addressed.

First a series of questions need to be addressed at the neural circuit level. As the dmPFC contains heterogeneous neural populations, it will be important to determine how cells of different types or with different projections within the dmPFC microcircuit differentially contribute to the control of social dominance. To understand how dmPFC regulates

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Kay Tye and anonymous reviewers for stimulating discussions and suggestions. This work was supported by the Natural Science Foundation of China (#91432108, #31225010, and #81527901) to H.H.

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    These authors contributed equally to this work.

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