Neural systems that facilitate the representation of social rank. Madeleine F. Dwortz, James P. Curley, Kay M. Tye and Nancy Padilla-Coreano. Philosophical Transactions of the Royal Society B: Biological Sciences, January 10 2022. https://doi.org/10.1098/rstb.2020.0444
Abstract: Across species, animals organize into social dominance hierarchies that serve to decrease aggression and facilitate survival of the group. Neuroscientists have adopted several model organisms to study dominance hierarchies in the laboratory setting, including fish, reptiles, rodents and primates. We review recent literature across species that sheds light onto how the brain represents social rank to guide socially appropriate behaviour within a dominance hierarchy. First, we discuss how the brain responds to social status signals. Then, we discuss social approach and avoidance learning mechanisms that we propose could drive rank-appropriate behaviour. Lastly, we discuss how the brain represents memories of individuals (social memory) and how this may support the maintenance of unique individual relationships within a social group.
5. Conclusion and future directions
The evidence reviewed supports that social rank recognition involves the coordinated activity of highly conserved neural circuits across multiple levels of cognition, ranging from the seemingly innate perception of social status signals to more fine-tuned learning of social rank of specific individuals. Notably, the amygdala and dopaminergic neurons are involved in responding to status signals and driving learning about social rank through social interactions. While it appears that status signals serve to bypass the need for experience-based learning and prior social interactions that could incur physical injury, the extent to which status signal responses are innate or learned needs to be more thoroughly investigated. This theory, along with several other critical questions about how the brain processes social status signals, needs to be further investigated. In particular, the impact of an animal's familiarity with a social stimulus on their perception of status signals needs to be systematically studied across species. In addition, the role of an animal's own social rank in modulating how they process external status signals is largely unknown. An individual's social rank appears to influence behaviours related to acquiring social information, such as attentional postures and visual gaze direction [3–9], but how social information is differentially represented in the brains of hierarchically ranked animals is understudied. Lastly and perhaps most glaringly absent from our knowledge is how the female brain represents social rank and the neural underpinnings of how females negotiate social rank relationships. Much of the knowledge presented in this review stems from experiments conducted almost exclusively in male animals.
The technical difficulty of studying proximal mechanisms of brain function in naturalistic contexts has been a major hurdle in studying such questions and has led to our limited knowledge of the neural dynamics underlying social group behaviours. Although the species discussed in this review form dominance hierarchies, evidence for the neural systems involved in the representation of social rank typically does not come directly from animals living and behaving freely in groups. Laboratory-based neurobiological and behavioural studies have an overrepresentation of simple dyadic social interaction assays that do not directly examine the representation of social rank in groups, and traditionally measure behaviours that are exclusively expressed by males. Moreover, traditional neural recording methods, such as electrophysiology, have been hard to implement in multiple freely moving animals because of physical constraints. Several recent technological advancements have increased our ability to study the neural basis of social rank learning and memory in larger and more natural group settings. In the past few years, open-source tools have been developed to automatically track and assist in the quantification of behaviour of multiple group-living animals [182–185]. Moreover, technological advancements in light wireless neural activity recording now allow recording from multiple freely moving animals simultaneously [186]. These new developments combined will dramatically facilitate the study of neural circuits and dynamics underlying social group behaviour. We anticipate that the next decade will bring new perspectives on the neurobiology of social group behaviours that will enhance our understanding of how animals in large groups learn and represent social rank.
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