The Emergence and Representation of Knowledge about Social and Nonsocial Hierarchies

Dharshan Kumaran,Hans Ludwig Melo,Emrah Duzel

doi:10.1016/j.neuron.2012.09.035

Dharshan Kumaran, Hans Ludwig Melo + Show 1 more

Open Access

https://doi.org/10.1016/j.neuron.2012.09.035

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Abstract

SummaryPrimates are remarkably adept at ranking each other within social hierarchies, a capacity that is critical to successful group living. Surprisingly little, however, is understood about the neurobiology underlying this quintessential aspect of primate cognition. In our experiment, participants first acquired knowledge about a social and a nonsocial hierarchy and then used this information to guide investment decisions. We found that neural activity in the amygdala tracked the development of knowledge about a social, but not a nonsocial, hierarchy. Further, structural variations in amygdala gray matter volume accounted for interindividual differences in social transitivity performance. Finally, the amygdala expressed a neural signal selectively coding for social rank, whose robustness predicted the influence of rank on participants’ investment decisions. In contrast, we observed that the linear structure of both social and nonsocial hierarchies was represented at a neural level in the hippocampus. Our study implicates the amygdala in the emergence and representation of knowledge about social hierarchies and distinguishes the domain-general contribution of the hippocampus.

Highlights

While the Learn phase paradigm builds on a rich vein of research that has used the transitive inference task across species (Bryant and Trabasso, 1971; Dusek and Eichenbaum, 1997; Greene et al, 2006; Grosenick et al, 2007; Heckers et al, 2004; Hurliman et al, 2005; Moses et al, 2010; PazY-Mino et al, 2004; Zeithamova et al, 2012), we incorporated several features designed to achieve the specific goals of our experiment: first, we interleaved blocks of training and test trials throughout the time course of the Learn phase in order to chart the development of successful transitive behavior
Our findings further demonstrate that neural activity in the amygdala selectively discloses the worth of other individuals based on their rank, a signal that could potentially be useful in guiding the selection of advantageous coalition partners (Cheney and Seyfarth, 1990; Tomasello and Call, 1997)
Primates possess sophisticated knowledge of the rank relations that exist between fellow members of their social group (Byrne and Bates, 2010; Cheney and Seyfarth, 1990; Tomasello and Call, 1997), yet surprisingly little is understood about the underlying neural mechanisms

Summary

Introduction

Primates have sophisticated cognitive abilities that enable individuals to meet the challenging pressures of living in large social groups (Byrne and Bates, 2010; Cheney and Seyfarth, 1990; Tomasello and Call, 1997). Primates spontaneously discriminate images of individuals based on their rank status (Deaner et al, 2005) and are able to identify third-party relations that exist between their companions—when engaged in a competitive interaction (e.g., a duel) individuals will typically recruit allies that outrank both themselves and their opponents (e.g., favoring the 3rd ranked individual over the fifth ranked) (Cheney and Seyfarth, 1990; Tomasello and Call, 1997)

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