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Cortical dynamics underlying social behavior in dominance hierarchy and spatial navigation

View ORCID ProfileAriel Lara-Vasquez, Nelson Espinosa, Cristian Morales, Constanza Moran, Pablo Billeke, Joseph Gallagher, Joshua J. Strohl, Patricio T. Huerta, Pablo Fuentealba
doi: https://doi.org/10.1101/2020.06.12.147249
Ariel Lara-Vasquez
aCentro Integrativo de Neurociencias y Departamento de Psiquiatría, Pontificia Universidad Católica de Chile, Santiago, Chile
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  • ORCID record for Ariel Lara-Vasquez
Nelson Espinosa
aCentro Integrativo de Neurociencias y Departamento de Psiquiatría, Pontificia Universidad Católica de Chile, Santiago, Chile
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Cristian Morales
aCentro Integrativo de Neurociencias y Departamento de Psiquiatría, Pontificia Universidad Católica de Chile, Santiago, Chile
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Constanza Moran
aCentro Integrativo de Neurociencias y Departamento de Psiquiatría, Pontificia Universidad Católica de Chile, Santiago, Chile
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Pablo Billeke
cLaboratorio de Neurociencia Social y Neuromodulación, Centro de Investigación en Complejidad Social, Universidad del Desarrollo, Santiago, Chile
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Joseph Gallagher
dLaboratory of Immune & Neural Networks, Feinstein Institutes for Medical Research, Manhasset, New York, USA
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Joshua J. Strohl
dLaboratory of Immune & Neural Networks, Feinstein Institutes for Medical Research, Manhasset, New York, USA
eDepartment of Molecular Medicine, Zucker School of Medicine at Hofstra/Northwell, Manhasset, New York, USA
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Patricio T. Huerta
dLaboratory of Immune & Neural Networks, Feinstein Institutes for Medical Research, Manhasset, New York, USA
eDepartment of Molecular Medicine, Zucker School of Medicine at Hofstra/Northwell, Manhasset, New York, USA
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Pablo Fuentealba
aCentro Integrativo de Neurociencias y Departamento de Psiquiatría, Pontificia Universidad Católica de Chile, Santiago, Chile
bCentro de Investigación en Nanotecnología y Materiales Avanzados - CIEN-UC, Pontificia Universidad Católica de Chile, Santiago, Chile
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  • For correspondence: pfuentealba@uc.cl
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Abstract

Rodents establish dominance hierarchy as a social ranking system in which one subject acts as dominant over all the other subordinate individuals. Dominance hierarchy regulates food access and mating opportunities, but little is known of its significance in collective behavior, for instance during navigation for foraging or migration. Here, we implemented a simplified goal-directed spatial navigation task in mice and found that the social context exerts significant influence on individual decision-making, even when efficient navigation rules leading to reward had been previously learned. Thus, decision-making and consequent task performance were strongly dependent on contingent social interactions arising during collective navigation, yet their influence on individual behavior was outlined by dominance hierarchy. Dominant animals did not behave as leaders during navigation; conversely, they were most sensitive to social context. Social ranking in turn was reflected in the neural activity and connectivity patterns of the prefrontal cortex and hippocampus, both in anesthetized and behaving mice. These results suggest that the interplay between contingent social interactions and dominance hierarchy can regulate behavioral performance, supported by the intrinsic matrix of coordinated activity in the hippocampal-prefrontal circuit.

Significance Statement Decision-making is shaped by intrinsic features, such as memory-stored information, and external influences, such as social interactions, yet their interplay is not well understood. We studied decision-making during collective behavior and found that instead of prioritizing memory-based pertinent information, mice shifted their individual decisions according to contingent social interactions arising in the social context. Conversely, constitutive social interactions, such as dominance hierarchy, were relevant to outline the effect of the social environment on individual behavior. Our results suggest that intrinsic hippocampal-cortical activity and connectivity patterns define social interactions. Hence, intrinsic cortical dynamics underlie behavioral performance during social decision-making.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Competing financial interests: The authors declare no competing financial interests

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 12, 2020.
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Cortical dynamics underlying social behavior in dominance hierarchy and spatial navigation
Ariel Lara-Vasquez, Nelson Espinosa, Cristian Morales, Constanza Moran, Pablo Billeke, Joseph Gallagher, Joshua J. Strohl, Patricio T. Huerta, Pablo Fuentealba
bioRxiv 2020.06.12.147249; doi: https://doi.org/10.1101/2020.06.12.147249
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Cortical dynamics underlying social behavior in dominance hierarchy and spatial navigation
Ariel Lara-Vasquez, Nelson Espinosa, Cristian Morales, Constanza Moran, Pablo Billeke, Joseph Gallagher, Joshua J. Strohl, Patricio T. Huerta, Pablo Fuentealba
bioRxiv 2020.06.12.147249; doi: https://doi.org/10.1101/2020.06.12.147249

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