Rescue-like behavior in a bystander mouse toward anesthetized conspecifics promotes arousal via a tongue-brain connection

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Abstract

Prosocial behaviors are advantageous to social species, but the neural mechanism(s) through which others receive benefit remain unknown. Here, we found that bystander mice display rescue-like behavior (tongue dragging) toward anesthetized cagemates and found that this tongue dragging promotes arousal from anesthesia through a direct tongue-brain circuit. We found that a direct circuit from the tongue → glutamatergic neurons in the mesencephalic trigeminal nucleus (MTN ^Glu) → noradrenergic neurons in the locus coeruleus (LC ^NE) drives rapid arousal in the anesthetized mice that receive the rescue-like behavior from bystanders. Artificial inhibition of this circuit abolishes the rapid arousal effect induced by the rescue-like behavior. Further, we revealed that glutamatergic neurons in the paraventricular nucleus of the thalamus (PVT ^Glu) that project to the nucleus accumbens shell (NAcSh) mediate the rescue-like behavior. These findings reveal a tongue-brain connection underlying the rapid arousal effects induced by rescue-like behavior and the circuit basis governing this specific form of prosocial behavior.

Abstract

Bystander mice exhibit rescue-like behavior, promoting arousal in anesthetized mice via a direct tongue-brain circuit.

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Most cited references 70

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Author and article information

Contributors

Peng Cao:

ORCID: https://orcid.org/0009-0001-6712-429X

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Ying Liu:

ORCID: https://orcid.org/0009-0004-0084-9087

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Ziyun Ni:

ORCID: https://orcid.org/0000-0002-1314-7963

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Validation

Mingjun Zhang:

ORCID: https://orcid.org/0000-0002-8483-8171

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Hong-Rui Wei:

ORCID: https://orcid.org/0000-0002-7511-1747

Role: Investigation

An Liu: Role: Investigation

Jin-Rong Guo: Role: MethodologyRole: Validation

Yumeng Yang:

ORCID: https://orcid.org/0009-0001-8801-185X

Role: Formal analysisRole: Visualization

Zheng Xu: Role: Methodology

Yuyu Guo: Role: Methodology

Zhi Zhang:

ORCID: https://orcid.org/0000-0002-4205-3181

Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Wenjuan Tao:

ORCID: https://orcid.org/0000-0002-0525-0514

Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Likui Wang:

ORCID: https://orcid.org/0000-0001-5376-351X

Role: ConceptualizationRole: Data curationRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: 24 January 2025

Publication date (Electronic, pub): 22 January 2025

Volume: 11

Issue: 4

Electronic Location Identifier: eadq3874

Affiliations

[ ¹ ]Department of Anesthesiology, The First Affiliated Hospital of USTC, Hefei National Laboratory for Physical Sciences at the Microscale, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China.

[ ² ]Department of Physiology, School of Basic Medical Sciences, Anhui Medical University, Hefei 230022, China.

[ ³ ]NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou 221004, China.

[ ⁴ ]Department of Pain Medicine, The First Affiliated Hospital of Anhui Medical University, Hefei 230022, China.

[ ⁵ ]College & Hospital of Stomatology, Key Laboratory of Oral Diseases Research of Anhui Province, Anhui Medical University, Hefei 230022, China.

Author notes

[* ]Corresponding author. Email: wjtao01@ 123456ahmu.edu.cn (W.T.); wlk9560@ 123456163.com (L.W.); zhizhang@ 123456ustc.edu.cn (Z.Z.)

[†]

These authors contributed equally to this work.

Author information

Peng Cao https://orcid.org/0009-0001-6712-429X

Ying Liu https://orcid.org/0009-0004-0084-9087

Ziyun Ni https://orcid.org/0000-0002-1314-7963

Mingjun Zhang https://orcid.org/0000-0002-8483-8171

Hong-Rui Wei https://orcid.org/0000-0002-7511-1747

Yumeng Yang https://orcid.org/0009-0001-8801-185X

Zhi Zhang https://orcid.org/0000-0002-4205-3181

Wenjuan Tao https://orcid.org/0000-0002-0525-0514

Likui Wang https://orcid.org/0000-0001-5376-351X

Article

Publisher ID: adq3874

DOI: 10.1126/sciadv.adq3874

PMC ID: 11753405

PubMed ID: 39841840

SO-VID: 557a7254-6496-4571-b39e-ee661dfbb2a2

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