Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability

Consolation is a common response to the distress of others in humans and some social animals, but the neural mechanisms underlying this behavior are not well characterized. By using socially monogamous mandarin voles, we found that optogenetic or chemogenetic inhibition of 5-HTergic neurons in the d...

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Main Authors: Laifu Li, Li-Zi Zhang, Zhi-Xiong He, Huan Ma, Yu-Ting Zhang, Yu-Feng Xun, Wei Yuan, Wen-Juan Hou, Yi-Tong Li, Zi-Jian Lv, Rui Jia, Fa-Dao Tai
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/67638
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author Laifu Li
Li-Zi Zhang
Zhi-Xiong He
Huan Ma
Yu-Ting Zhang
Yu-Feng Xun
Wei Yuan
Wen-Juan Hou
Yi-Tong Li
Zi-Jian Lv
Rui Jia
Fa-Dao Tai
author_facet Laifu Li
Li-Zi Zhang
Zhi-Xiong He
Huan Ma
Yu-Ting Zhang
Yu-Feng Xun
Wei Yuan
Wen-Juan Hou
Yi-Tong Li
Zi-Jian Lv
Rui Jia
Fa-Dao Tai
author_sort Laifu Li
collection DOAJ
description Consolation is a common response to the distress of others in humans and some social animals, but the neural mechanisms underlying this behavior are not well characterized. By using socially monogamous mandarin voles, we found that optogenetic or chemogenetic inhibition of 5-HTergic neurons in the dorsal raphe nucleus (DR) or optogenetic inhibition of serotonin (5-HT) terminals in the anterior cingulate cortex (ACC) significantly decreased allogrooming time in the consolation test and reduced sociability in the three-chamber test. The release of 5-HT within the ACC and the activity of DR neurons were significantly increased during allogrooming, sniffing, and social approaching. Finally, we found that the activation of 5-HT1A receptors in the ACC was sufficient to reverse consolation and sociability deficits induced by the chemogenetic inhibition of 5-HTergic neurons in the DR. Our study provided the first direct evidence that DR-ACC 5-HTergic neural circuit is implicated in consolation-like behaviors and sociability.
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spelling doaj.art-cbddec1f36954c11becb22923c3b6ff22022-12-22T04:32:39ZengeLife Sciences Publications LtdeLife2050-084X2021-06-011010.7554/eLife.67638Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociabilityLaifu Li0Li-Zi Zhang1Zhi-Xiong He2Huan Ma3Yu-Ting Zhang4Yu-Feng Xun5Wei Yuan6Wen-Juan Hou7Yi-Tong Li8Zi-Jian Lv9Rui Jia10Fa-Dao Tai11https://orcid.org/0000-0002-6804-4179Institute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, China; College of Life Sciences, Nanyang Normal University, Nanyang, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, China; Provincial Key Laboratory of Acupuncture and Medications, Shaanxi University of Chinese Medicine, Xianyang, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaInstitute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, ChinaConsolation is a common response to the distress of others in humans and some social animals, but the neural mechanisms underlying this behavior are not well characterized. By using socially monogamous mandarin voles, we found that optogenetic or chemogenetic inhibition of 5-HTergic neurons in the dorsal raphe nucleus (DR) or optogenetic inhibition of serotonin (5-HT) terminals in the anterior cingulate cortex (ACC) significantly decreased allogrooming time in the consolation test and reduced sociability in the three-chamber test. The release of 5-HT within the ACC and the activity of DR neurons were significantly increased during allogrooming, sniffing, and social approaching. Finally, we found that the activation of 5-HT1A receptors in the ACC was sufficient to reverse consolation and sociability deficits induced by the chemogenetic inhibition of 5-HTergic neurons in the DR. Our study provided the first direct evidence that DR-ACC 5-HTergic neural circuit is implicated in consolation-like behaviors and sociability.https://elifesciences.org/articles/67638consolationempathyanterior cingulate cortexserotoninmandarin volesdorsal raphe nucleus
spellingShingle Laifu Li
Li-Zi Zhang
Zhi-Xiong He
Huan Ma
Yu-Ting Zhang
Yu-Feng Xun
Wei Yuan
Wen-Juan Hou
Yi-Tong Li
Zi-Jian Lv
Rui Jia
Fa-Dao Tai
Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability
eLife
consolation
empathy
anterior cingulate cortex
serotonin
mandarin voles
dorsal raphe nucleus
title Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability
title_full Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability
title_fullStr Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability
title_full_unstemmed Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability
title_short Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability
title_sort dorsal raphe nucleus to anterior cingulate cortex 5 htergic neural circuit modulates consolation and sociability
topic consolation
empathy
anterior cingulate cortex
serotonin
mandarin voles
dorsal raphe nucleus
url https://elifesciences.org/articles/67638
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