Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formation

Abstract The social stress often induces fear memory and stress-relevant phobias. Molecular and cellular mechanisms of fear memory and anxiety remain to be addressed for the exploration of therapeutic strategies for these deficits. In social defeat mice induced by the resident/intruder paradigm, we...

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Main Authors: Yun Zhang, Bingchen Chen, Jiayi Li, Lei Wang, Yang Xu, Jin-Hui Wang
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-025-03357-9
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author Yun Zhang
Bingchen Chen
Jiayi Li
Lei Wang
Yang Xu
Jin-Hui Wang
author_facet Yun Zhang
Bingchen Chen
Jiayi Li
Lei Wang
Yang Xu
Jin-Hui Wang
author_sort Yun Zhang
collection DOAJ
description Abstract The social stress often induces fear memory and stress-relevant phobias. Molecular and cellular mechanisms of fear memory and anxiety remain to be addressed for the exploration of therapeutic strategies for these deficits. In social defeat mice induced by the resident/intruder paradigm, we have examined how auditory cortical neurons are recruited to encode stress signals that cause fear memory and anxiety by approaches of behavioral tasks, neural tracing, electrophysiology and molecular biology. The social stress in intruder C57 mice by the attack of resident CD1 mouse causes their fear memory and anxiety-like behaviors. In addition to the interconnections between auditory and somatosensory cortices in the mice of fear memory and anxiety, auditory cortical neurons receive new synapses from the somatosensory cortex and the synapses from the medial geniculate body. These auditory cortical neurons are able to encode the stress signals including the pain stimulus to injury areas and the battle sound in a resident/intruder paradigm. Neuroligin-3 mRNA knockdown in the auditory cortex prevents the recruitment of associative memory neurons that encode fear memory and anxiety-like behaviors. Therefore, neuroligin3-mediated synapse formation is essential for the stress-induced recruitment of associative memory neurons in auditory cortices that encode stress signals, fear memory and anxiety.
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issn 2158-3188
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publishDate 2025-04-01
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series Translational Psychiatry
spelling doaj-art-3f26f08f069f4b2399781172e8d03e9c2025-08-20T02:17:05ZengNature Publishing GroupTranslational Psychiatry2158-31882025-04-0115111510.1038/s41398-025-03357-9Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formationYun Zhang0Bingchen Chen1Jiayi Li2Lei Wang3Yang Xu4Jin-Hui Wang5College of Life Science, University of Chinese Academy of SciencesCollege of Life Science, University of Chinese Academy of SciencesCollege of Life Science, University of Chinese Academy of SciencesCollege of Life Science, University of Chinese Academy of SciencesCollege of Life Science, University of Chinese Academy of SciencesCollege of Life Science, University of Chinese Academy of SciencesAbstract The social stress often induces fear memory and stress-relevant phobias. Molecular and cellular mechanisms of fear memory and anxiety remain to be addressed for the exploration of therapeutic strategies for these deficits. In social defeat mice induced by the resident/intruder paradigm, we have examined how auditory cortical neurons are recruited to encode stress signals that cause fear memory and anxiety by approaches of behavioral tasks, neural tracing, electrophysiology and molecular biology. The social stress in intruder C57 mice by the attack of resident CD1 mouse causes their fear memory and anxiety-like behaviors. In addition to the interconnections between auditory and somatosensory cortices in the mice of fear memory and anxiety, auditory cortical neurons receive new synapses from the somatosensory cortex and the synapses from the medial geniculate body. These auditory cortical neurons are able to encode the stress signals including the pain stimulus to injury areas and the battle sound in a resident/intruder paradigm. Neuroligin-3 mRNA knockdown in the auditory cortex prevents the recruitment of associative memory neurons that encode fear memory and anxiety-like behaviors. Therefore, neuroligin3-mediated synapse formation is essential for the stress-induced recruitment of associative memory neurons in auditory cortices that encode stress signals, fear memory and anxiety.https://doi.org/10.1038/s41398-025-03357-9
spellingShingle Yun Zhang
Bingchen Chen
Jiayi Li
Lei Wang
Yang Xu
Jin-Hui Wang
Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formation
Translational Psychiatry
title Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formation
title_full Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formation
title_fullStr Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formation
title_full_unstemmed Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formation
title_short Auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin-3-mediated synapse formation
title_sort auditory cortical neurons are recruited to encode fear signals and anxiety by neuroligin 3 mediated synapse formation
url https://doi.org/10.1038/s41398-025-03357-9
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AT jiayili auditorycorticalneuronsarerecruitedtoencodefearsignalsandanxietybyneuroligin3mediatedsynapseformation
AT leiwang auditorycorticalneuronsarerecruitedtoencodefearsignalsandanxietybyneuroligin3mediatedsynapseformation
AT yangxu auditorycorticalneuronsarerecruitedtoencodefearsignalsandanxietybyneuroligin3mediatedsynapseformation
AT jinhuiwang auditorycorticalneuronsarerecruitedtoencodefearsignalsandanxietybyneuroligin3mediatedsynapseformation