A neural circuit covarying with social hierarchy in macaques.

Despite widespread interest in social dominance, little is known of its neural correlates in primates. We hypothesized that social status in primates might be related to individual variation in subcortical brain regions implicated in other aspects of social and emotional behavior in other mammals. T...

Full description

Saved in:
Bibliographic Details
Main Authors: MaryAnn P Noonan, Jerome Sallet, Rogier B Mars, Franz X Neubert, Jill X O'Reilly, Jesper L Andersson, Anna S Mitchell, Andrew H Bell, Karla L Miller, Matthew F S Rushworth
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-09-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.1001940
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849726877068951552
author MaryAnn P Noonan
Jerome Sallet
Rogier B Mars
Franz X Neubert
Jill X O'Reilly
Jesper L Andersson
Anna S Mitchell
Andrew H Bell
Karla L Miller
Matthew F S Rushworth
author_facet MaryAnn P Noonan
Jerome Sallet
Rogier B Mars
Franz X Neubert
Jill X O'Reilly
Jesper L Andersson
Anna S Mitchell
Andrew H Bell
Karla L Miller
Matthew F S Rushworth
author_sort MaryAnn P Noonan
collection DOAJ
description Despite widespread interest in social dominance, little is known of its neural correlates in primates. We hypothesized that social status in primates might be related to individual variation in subcortical brain regions implicated in other aspects of social and emotional behavior in other mammals. To examine this possibility we used magnetic resonance imaging (MRI), which affords the taking of quantitative measurements noninvasively, both of brain structure and of brain function, across many regions simultaneously. We carried out a series of tests of structural and functional MRI (fMRI) data in 25 group-living macaques. First, a deformation-based morphometric (DBM) approach was used to show that gray matter in the amygdala, brainstem in the vicinity of the raphe nucleus, and reticular formation, hypothalamus, and septum/striatum of the left hemisphere was correlated with social status. Second, similar correlations were found in the same areas in the other hemisphere. Third, similar correlations were found in a second data set acquired several months later from a subset of the same animals. Fourth, the strength of coupling between fMRI-measured activity in the same areas was correlated with social status. The network of subcortical areas, however, had no relationship with the sizes of individuals' social networks, suggesting the areas had a simple and direct relationship with social status. By contrast a second circuit in cortex, comprising the midsuperior temporal sulcus and anterior and dorsal prefrontal cortex, covaried with both individuals' social statuses and the social network sizes they experienced. This cortical circuit may be linked to the social cognitive processes that are taxed by life in more complex social networks and that must also be used if an animal is to achieve a high social status.
format Article
id doaj-art-10326f5daf4f48dc90a53fbb4b3b4870
institution DOAJ
issn 1544-9173
1545-7885
language English
publishDate 2014-09-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj-art-10326f5daf4f48dc90a53fbb4b3b48702025-08-20T03:10:02ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852014-09-01129e100194010.1371/journal.pbio.1001940A neural circuit covarying with social hierarchy in macaques.MaryAnn P NoonanJerome SalletRogier B MarsFranz X NeubertJill X O'ReillyJesper L AnderssonAnna S MitchellAndrew H BellKarla L MillerMatthew F S RushworthDespite widespread interest in social dominance, little is known of its neural correlates in primates. We hypothesized that social status in primates might be related to individual variation in subcortical brain regions implicated in other aspects of social and emotional behavior in other mammals. To examine this possibility we used magnetic resonance imaging (MRI), which affords the taking of quantitative measurements noninvasively, both of brain structure and of brain function, across many regions simultaneously. We carried out a series of tests of structural and functional MRI (fMRI) data in 25 group-living macaques. First, a deformation-based morphometric (DBM) approach was used to show that gray matter in the amygdala, brainstem in the vicinity of the raphe nucleus, and reticular formation, hypothalamus, and septum/striatum of the left hemisphere was correlated with social status. Second, similar correlations were found in the same areas in the other hemisphere. Third, similar correlations were found in a second data set acquired several months later from a subset of the same animals. Fourth, the strength of coupling between fMRI-measured activity in the same areas was correlated with social status. The network of subcortical areas, however, had no relationship with the sizes of individuals' social networks, suggesting the areas had a simple and direct relationship with social status. By contrast a second circuit in cortex, comprising the midsuperior temporal sulcus and anterior and dorsal prefrontal cortex, covaried with both individuals' social statuses and the social network sizes they experienced. This cortical circuit may be linked to the social cognitive processes that are taxed by life in more complex social networks and that must also be used if an animal is to achieve a high social status.https://doi.org/10.1371/journal.pbio.1001940
spellingShingle MaryAnn P Noonan
Jerome Sallet
Rogier B Mars
Franz X Neubert
Jill X O'Reilly
Jesper L Andersson
Anna S Mitchell
Andrew H Bell
Karla L Miller
Matthew F S Rushworth
A neural circuit covarying with social hierarchy in macaques.
PLoS Biology
title A neural circuit covarying with social hierarchy in macaques.
title_full A neural circuit covarying with social hierarchy in macaques.
title_fullStr A neural circuit covarying with social hierarchy in macaques.
title_full_unstemmed A neural circuit covarying with social hierarchy in macaques.
title_short A neural circuit covarying with social hierarchy in macaques.
title_sort neural circuit covarying with social hierarchy in macaques
url https://doi.org/10.1371/journal.pbio.1001940
work_keys_str_mv AT maryannpnoonan aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT jeromesallet aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT rogierbmars aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT franzxneubert aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT jillxoreilly aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT jesperlandersson aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT annasmitchell aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT andrewhbell aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT karlalmiller aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT matthewfsrushworth aneuralcircuitcovaryingwithsocialhierarchyinmacaques
AT maryannpnoonan neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT jeromesallet neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT rogierbmars neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT franzxneubert neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT jillxoreilly neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT jesperlandersson neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT annasmitchell neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT andrewhbell neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT karlalmiller neuralcircuitcovaryingwithsocialhierarchyinmacaques
AT matthewfsrushworth neuralcircuitcovaryingwithsocialhierarchyinmacaques