Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in mice

IntroductionBrachial plexus avulsion (BPA) injury develops frequent and intense neuropathic pain, involving in both peripheral and central nervous systems. The incidence of anxiety or depression caused by BPA-induced neuropathic pain is high, but the underlying mechanism remains unclear.MethodsWe es...

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Main Authors: Jian-lei Zhang, Hang Xian, Rui Zhao, Ceng Luo, Rou-gang Xie, Tong Tian, Rui Cong
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2023.1084494/full
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author Jian-lei Zhang
Hang Xian
Rui Zhao
Ceng Luo
Rou-gang Xie
Tong Tian
Rui Cong
author_facet Jian-lei Zhang
Hang Xian
Rui Zhao
Ceng Luo
Rou-gang Xie
Tong Tian
Rui Cong
author_sort Jian-lei Zhang
collection DOAJ
description IntroductionBrachial plexus avulsion (BPA) injury develops frequent and intense neuropathic pain, involving in both peripheral and central nervous systems. The incidence of anxiety or depression caused by BPA-induced neuropathic pain is high, but the underlying mechanism remains unclear.MethodsWe established a BPA mice model and assessed its negative emotions through behavioral tests. To further explore the role of the microbiota-gut-brain axis in the unique emotional behavior after BPA, we performed intestinal fecal 16s and metabolomics assays. Psychobiotics (PB) supplementation was administered to BPA mice to check the probiotics effects on BPA-induced anxiety behaviors.ResultsPain related anxiety-like behavior was observed at the early stage after BPA (7 days), while no depression-like behavior was detected. Intriguingly, gut microbiota diversity was increased in BPA mice, and the most abundant probiotics, Lactobacillus, showed obvious changes. Lactobacillus_reuteri was significantly decreased in BPA mice. Metabolomics analysis showed that Lactobacillus_reuteri-related bile acid pathway and some neurotransmitter amino acids were significantly altered. Further PB (dominated by Lactobacillus_reuteri) supplementation could significantly relieve BPA-induced anxiety-like behaviors in mice.ConclusionOur study suggests that pathological neuralgia after BPA could alter intestinal microbiota diversity, especially Lactobacillus, and the changes in neurotransmitter amino acid metabolites may be the key reason for the onset of anxiety-like behaviors in BPA mice.
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spelling doaj.art-dd01bf95bb0644ea8ff369bf5d107b522023-02-08T06:09:31ZengFrontiers Media S.A.Frontiers in Neurology1664-22952023-02-011410.3389/fneur.2023.10844941084494Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in miceJian-lei Zhang0Hang Xian1Rui Zhao2Ceng Luo3Rou-gang Xie4Tong Tian5Rui Cong6Department of Orthopedics, Xijing Hospital, Air Force Medical University, Xi'an, ChinaDepartment of Orthopedics, Xijing Hospital, Air Force Medical University, Xi'an, ChinaDepartment of Orthopedics, Xijing Hospital, Air Force Medical University, Xi'an, ChinaDepartment of Neurobiology, School of Basic Medicine, Air Force Medical University, Xi'an, ChinaDepartment of Neurobiology, School of Basic Medicine, Air Force Medical University, Xi'an, ChinaDepartment of Orthopedics, Xijing Hospital, Air Force Medical University, Xi'an, ChinaDepartment of Orthopedics, Xijing Hospital, Air Force Medical University, Xi'an, ChinaIntroductionBrachial plexus avulsion (BPA) injury develops frequent and intense neuropathic pain, involving in both peripheral and central nervous systems. The incidence of anxiety or depression caused by BPA-induced neuropathic pain is high, but the underlying mechanism remains unclear.MethodsWe established a BPA mice model and assessed its negative emotions through behavioral tests. To further explore the role of the microbiota-gut-brain axis in the unique emotional behavior after BPA, we performed intestinal fecal 16s and metabolomics assays. Psychobiotics (PB) supplementation was administered to BPA mice to check the probiotics effects on BPA-induced anxiety behaviors.ResultsPain related anxiety-like behavior was observed at the early stage after BPA (7 days), while no depression-like behavior was detected. Intriguingly, gut microbiota diversity was increased in BPA mice, and the most abundant probiotics, Lactobacillus, showed obvious changes. Lactobacillus_reuteri was significantly decreased in BPA mice. Metabolomics analysis showed that Lactobacillus_reuteri-related bile acid pathway and some neurotransmitter amino acids were significantly altered. Further PB (dominated by Lactobacillus_reuteri) supplementation could significantly relieve BPA-induced anxiety-like behaviors in mice.ConclusionOur study suggests that pathological neuralgia after BPA could alter intestinal microbiota diversity, especially Lactobacillus, and the changes in neurotransmitter amino acid metabolites may be the key reason for the onset of anxiety-like behaviors in BPA mice.https://www.frontiersin.org/articles/10.3389/fneur.2023.1084494/fullbrachial plexus avulsionmicrobiota-gut-brain axismetabolitesanxietypsychobiotics
spellingShingle Jian-lei Zhang
Hang Xian
Rui Zhao
Ceng Luo
Rou-gang Xie
Tong Tian
Rui Cong
Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in mice
Frontiers in Neurology
brachial plexus avulsion
microbiota-gut-brain axis
metabolites
anxiety
psychobiotics
title Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in mice
title_full Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in mice
title_fullStr Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in mice
title_full_unstemmed Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in mice
title_short Brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety-like behavior in mice
title_sort brachial plexus avulsion induced changes in gut microbiota promotes pain related anxiety like behavior in mice
topic brachial plexus avulsion
microbiota-gut-brain axis
metabolites
anxiety
psychobiotics
url https://www.frontiersin.org/articles/10.3389/fneur.2023.1084494/full
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