The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and Depression

Abstract The locus coeruleus (LC) noradrenergic (NA) neurons regulate pain and depression through their projections to various downstream nuclei. Although GABAergic (GABA) neurons in and near the LC (LC‐GABA neurons) provide inhibitory synaptic inputs to LC‐NA neurons, it remains unknown whether the...

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Main Authors: Yuan Gao, Xue Zhang, Xiao‐Juan Liu, Yi‐Ling Sun, Cui Yin, Dong‐Liang Tang, Cheng Xiao, Chunyi Zhou
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202503739
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author Yuan Gao
Xue Zhang
Xiao‐Juan Liu
Yi‐Ling Sun
Cui Yin
Dong‐Liang Tang
Cheng Xiao
Chunyi Zhou
author_facet Yuan Gao
Xue Zhang
Xiao‐Juan Liu
Yi‐Ling Sun
Cui Yin
Dong‐Liang Tang
Cheng Xiao
Chunyi Zhou
author_sort Yuan Gao
collection DOAJ
description Abstract The locus coeruleus (LC) noradrenergic (NA) neurons regulate pain and depression through their projections to various downstream nuclei. Although GABAergic (GABA) neurons in and near the LC (LC‐GABA neurons) provide inhibitory synaptic inputs to LC‐NA neurons, it remains unknown whether they are implicated in neuropathic pain and comorbid depression through LC‐NA neurons. This study demonstrates that LC‐GABA neurons respond to noxious stimuli with enhanced activity, and stimulation of these neurons elevates pain thresholds and exerts an anti‐depressant‐like effect in naive and neuropathic pain mice. Conversely, inhibition of LC‐GABA neurons leads to hyperalgesia and depression‐like behaviors in naive mice and exacerbates existing pain‐ and depression‐like behaviors in neuropathic pain mice. Although LC‐GABA neurons inhibit pain responses in LC‐NA neurons, they modulate pain thresholds and depression‐like behaviors in a manner independent of LC‐NA neurons. In contrast, the projection from LC‐GABA neurons to the ventrolateral periaqueductal gray (vlPAG) is enhanced, and stimulation of this projection mimics that of LC‐GABA neurons conferring analgesic‐ and antidepressant‐like effects. This study reveals the enhancement of the LCGABA‐vlPAGGABA projection as a compensatory mechanism in neuropathic pain and suggests that further augmentation of this projection may be a therapeutic strategy for the treatment of comorbid neuropathic pain and depression.
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spelling doaj-art-6860b8aeb23240798060f39b7b9bc5ed2025-08-20T04:01:01ZengWileyAdvanced Science2198-38442025-07-011226n/an/a10.1002/advs.202503739The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and DepressionYuan Gao0Xue Zhang1Xiao‐Juan Liu2Yi‐Ling Sun3Cui Yin4Dong‐Liang Tang5Cheng Xiao6Chunyi Zhou7Jiangsu Province Key Laboratory of Anesthesiology School of Anesthesiology Xuzhou Medical University Xuzhou Jiangsu 221004 ChinaJiangsu Province Key Laboratory of Anesthesiology School of Anesthesiology Xuzhou Medical University Xuzhou Jiangsu 221004 ChinaJiangsu Province Key Laboratory of Anesthesiology School of Anesthesiology Xuzhou Medical University Xuzhou Jiangsu 221004 ChinaJiangsu Province Key Laboratory of Anesthesiology School of Anesthesiology Xuzhou Medical University Xuzhou Jiangsu 221004 ChinaJiangsu Province Key Laboratory of Anesthesiology School of Anesthesiology Xuzhou Medical University Xuzhou Jiangsu 221004 ChinaDepartment of Anesthesiology Nanjing Drum Tower Hospital Affiliated Hospital of Medical School, Nanjing University Nanjing Jiangsu 210008 ChinaJiangsu Province Key Laboratory of Anesthesiology School of Anesthesiology Xuzhou Medical University Xuzhou Jiangsu 221004 ChinaJiangsu Province Key Laboratory of Anesthesiology School of Anesthesiology Xuzhou Medical University Xuzhou Jiangsu 221004 ChinaAbstract The locus coeruleus (LC) noradrenergic (NA) neurons regulate pain and depression through their projections to various downstream nuclei. Although GABAergic (GABA) neurons in and near the LC (LC‐GABA neurons) provide inhibitory synaptic inputs to LC‐NA neurons, it remains unknown whether they are implicated in neuropathic pain and comorbid depression through LC‐NA neurons. This study demonstrates that LC‐GABA neurons respond to noxious stimuli with enhanced activity, and stimulation of these neurons elevates pain thresholds and exerts an anti‐depressant‐like effect in naive and neuropathic pain mice. Conversely, inhibition of LC‐GABA neurons leads to hyperalgesia and depression‐like behaviors in naive mice and exacerbates existing pain‐ and depression‐like behaviors in neuropathic pain mice. Although LC‐GABA neurons inhibit pain responses in LC‐NA neurons, they modulate pain thresholds and depression‐like behaviors in a manner independent of LC‐NA neurons. In contrast, the projection from LC‐GABA neurons to the ventrolateral periaqueductal gray (vlPAG) is enhanced, and stimulation of this projection mimics that of LC‐GABA neurons conferring analgesic‐ and antidepressant‐like effects. This study reveals the enhancement of the LCGABA‐vlPAGGABA projection as a compensatory mechanism in neuropathic pain and suggests that further augmentation of this projection may be a therapeutic strategy for the treatment of comorbid neuropathic pain and depression.https://doi.org/10.1002/advs.202503739depressionGABAergic neuronlocus coeruleusneuropathic painnoradrenergic neuronventrolateral periaqueductal gray
spellingShingle Yuan Gao
Xue Zhang
Xiao‐Juan Liu
Yi‐Ling Sun
Cui Yin
Dong‐Liang Tang
Cheng Xiao
Chunyi Zhou
The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and Depression
Advanced Science
depression
GABAergic neuron
locus coeruleus
neuropathic pain
noradrenergic neuron
ventrolateral periaqueductal gray
title The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and Depression
title_full The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and Depression
title_fullStr The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and Depression
title_full_unstemmed The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and Depression
title_short The Locus Coeruleus‐Periaqueductal Gray GABAergic Projection Regulates Comorbid Pain and Depression
title_sort locus coeruleus periaqueductal gray gabaergic projection regulates comorbid pain and depression
topic depression
GABAergic neuron
locus coeruleus
neuropathic pain
noradrenergic neuron
ventrolateral periaqueductal gray
url https://doi.org/10.1002/advs.202503739
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