Dynamical Representation of Dominance Relationships in the Human Rostromedial Prefrontal Cortex

Humans and other primates have evolved the ability to represent their status in the group’s social hierarchy, which is essential for avoiding harm and accessing resources. Yet it remains unclear how the human brain learns dominance status and adjusts behavior accordingly during dynamic social intera...

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Published inCurrent biology Vol. 26; no. 23; pp. 3107 - 3115
Main Authors Ligneul, Romain, Obeso, Ignacio, Ruff, Christian C., Dreher, Jean-Claude
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 05.12.2016
Elsevier
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Abstract Humans and other primates have evolved the ability to represent their status in the group’s social hierarchy, which is essential for avoiding harm and accessing resources. Yet it remains unclear how the human brain learns dominance status and adjusts behavior accordingly during dynamic social interactions. Here we address this issue with a combination of fMRI and transcranial direct current stimulation (tDCS). In a first fMRI experiment, participants learned an implicit dominance hierarchy while playing a competitive game against three opponents of different skills. Neural activity in the rostromedial PFC (rmPFC) dynamically tracked and updated the dominance status of the opponents, whereas the ventromedial PFC and ventral striatum reacted specifically to competitive victories and defeats. In a second experiment, we applied anodal tDCS over the rmPFC to enhance neural excitability while subjects performed a similar competitive task. The stimulation enhanced the relative weight of victories over defeats in learning social dominance relationships and exacerbated the influence of one’s own dominance over competitive strategies. Importantly, these tDCS effects were specific to trials in which subjects learned about dominance relationships, as they were not present for control choices associated with monetary incentives but no competitive feedback. Taken together, our findings elucidate the role of rmPFC computations in dominance learning and unravel a fundamental mechanism that governs the emergence and maintenance of social dominance relationships in humans. [Display omitted] •Social dominance is learned by a reinforcement-learning process•Social dominance status and associated prediction errors are encoded in the rmPFC•rmPFC stimulation shifts the weight of victories and defeats for dominance learning Ligneul et al. demonstrate that BOLD activity in the rmPFC represents social dominance relationships as learned from competitive interactions, whereas the vmPFC and ventral striatum encode social victories and defeats, respectively. Electrical stimulation of the rmPFC modulates learning and updating of social dominance representations.
AbstractList Humans and other primates have evolved the ability to represent their status in the group's social hierarchy, which is essential for avoiding harm and accessing resources. Yet it remains unclear how the human brain learns dominance status and adjusts behavior accordingly during dynamic social interactions. Here we address this issue with a combination of fMRI and transcranial direct current stimulation (tDCS). In a first fMRI experiment, participants learned an implicit dominance hierarchy while playing a competitive game against three opponents of different skills. Neural activity in the rostromedial PFC (rmPFC) dynamically tracked and updated the dominance status of the opponents, whereas the ventromedial PFC and ventral striatum reacted specifically to competitive victories and defeats. In a second experiment, we applied anodal tDCS over the rmPFC to enhance neural excitability while subjects performed a similar competitive task. The stimulation enhanced the relative weight of victories over defeats in learning social dominance relationships and exacerbated the influence of one's own dominance over competitive strategies. Importantly, these tDCS effects were specific to trials in which subjects learned about dominance relationships, as they were not present for control choices associated with monetary incentives but no competitive feedback. Taken together, our findings elucidate the role of rmPFC computations in dominance learning and unravel a fundamental mechanism that governs the emergence and maintenance of social dominance relationships in humans.
Humans and other primates have evolved the ability to represent their status in the group’s social hierarchy, which is essential for avoiding harm and accessing resources. Yet it remains unclear how the human brain learns dominance status and adjusts behavior accordingly during dynamic social interactions. Here we address this issue with a combination of fMRI and transcranial direct current stimulation (tDCS). In a first fMRI experiment, participants learned an implicit dominance hierarchy while playing a competitive game against three opponents of different skills. Neural activity in the rostromedial PFC (rmPFC) dynamically tracked and updated the dominance status of the opponents, whereas the ventromedial PFC and ventral striatum reacted specifically to competitive victories and defeats. In a second experiment, we applied anodal tDCS over the rmPFC to enhance neural excitability while subjects performed a similar competitive task. The stimulation enhanced the relative weight of victories over defeats in learning social dominance relationships and exacerbated the influence of one’s own dominance over competitive strategies. Importantly, these tDCS effects were specific to trials in which subjects learned about dominance relationships, as they were not present for control choices associated with monetary incentives but no competitive feedback. Taken together, our findings elucidate the role of rmPFC computations in dominance learning and unravel a fundamental mechanism that governs the emergence and maintenance of social dominance relationships in humans. [Display omitted] •Social dominance is learned by a reinforcement-learning process•Social dominance status and associated prediction errors are encoded in the rmPFC•rmPFC stimulation shifts the weight of victories and defeats for dominance learning Ligneul et al. demonstrate that BOLD activity in the rmPFC represents social dominance relationships as learned from competitive interactions, whereas the vmPFC and ventral striatum encode social victories and defeats, respectively. Electrical stimulation of the rmPFC modulates learning and updating of social dominance representations.
Author Ligneul, Romain
Obeso, Ignacio
Ruff, Christian C.
Dreher, Jean-Claude
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Keywords social dominance
fMRI
reinforcement-learning
mPFC
performance
tDCS
ventral striatum
locus of control
social learning
social hierarchy
Language English
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Snippet Humans and other primates have evolved the ability to represent their status in the group’s social hierarchy, which is essential for avoiding harm and...
Humans and other primates have evolved the ability to represent their status in the group's social hierarchy, which is essential for avoiding harm and...
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SubjectTerms Cognitive science
Electric Stimulation
fMRI
Humans
Learning
locus of control
Magnetic Resonance Imaging
mPFC
Neuroscience
Prefrontal Cortex - anatomy & histology
Prefrontal Cortex - diagnostic imaging
Prefrontal Cortex - physiology
reinforcement-learning
Social Dominance
social hierarchy
social learning
tDCS
ventral striatum
Title Dynamical Representation of Dominance Relationships in the Human Rostromedial Prefrontal Cortex
URI https://dx.doi.org/10.1016/j.cub.2016.09.015
https://www.ncbi.nlm.nih.gov/pubmed/28094034
https://search.proquest.com/docview/1861558680
https://hal.science/hal-02341009
Volume 26
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