Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal Clostridiales

The relationship between the microbiota profile and exposure to stress is not well understood. Therefore, we used a rat model of unpredictable chronic mild stress (UCMS) to investigate this relationship. Depressive-like behaviors were measured in Female Sprague Dawley rats using the sucrose preferen...

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Main Authors: Tracey Bear, Nicole Roy, Julie Dalziel, Chrissie Butts, Jane Coad, Wayne Young, Shanthi G. Parkar, Duncan Hedderley, Hannah Dinnan, Sheridan Martell, Susanne Middlemiss-Kraak, Pramod Gopal
Format: Article
Language:English
Published: MDPI AG 2023-07-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/11/7/1773
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author Tracey Bear
Nicole Roy
Julie Dalziel
Chrissie Butts
Jane Coad
Wayne Young
Shanthi G. Parkar
Duncan Hedderley
Hannah Dinnan
Sheridan Martell
Susanne Middlemiss-Kraak
Pramod Gopal
author_facet Tracey Bear
Nicole Roy
Julie Dalziel
Chrissie Butts
Jane Coad
Wayne Young
Shanthi G. Parkar
Duncan Hedderley
Hannah Dinnan
Sheridan Martell
Susanne Middlemiss-Kraak
Pramod Gopal
author_sort Tracey Bear
collection DOAJ
description The relationship between the microbiota profile and exposure to stress is not well understood. Therefore, we used a rat model of unpredictable chronic mild stress (UCMS) to investigate this relationship. Depressive-like behaviors were measured in Female Sprague Dawley rats using the sucrose preference test and the Porsolt swim test. Anxiety-like behaviors were measured with the light–dark box test. Fecal corticosterone, cecal microbiota (composition and organic acids), plasma gut permeability (lipopolysaccharide-binding protein, LBP) and plasma inflammation (12 cytokines) markers were measured. Atypical behaviors were observed in female rats following UCMS, but no depressive-like behaviors were observed. Circulating concentrations of cytokines granulocyte-macrophage colony-stimulating factor and cytokine-induced neutrophil chemoattractant 1 were higher in UCMS-exposed female rats; plasma LBP and cecal organic acid levels remained unchanged. Our results reflect a resilient and adaptive phenotype for female SD rats. The relative abundance of taxa from the Clostridiales order and <i>Desulfovibrionaceae</i> family did, however, correlate both positively and negatively with anxiety-like behaviors and plasma cytokine concentrations, regardless of UCMS exposure, supporting the brain-to-gut influence of mild anxiety with a microbiota profile that may involve inflammatory pathways.
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spelling doaj.art-88e272946f0a40c7a43f1500f95409c62023-11-18T20:36:14ZengMDPI AGMicroorganisms2076-26072023-07-01117177310.3390/microorganisms11071773Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal ClostridialesTracey Bear0Nicole Roy1Julie Dalziel2Chrissie Butts3Jane Coad4Wayne Young5Shanthi G. Parkar6Duncan Hedderley7Hannah Dinnan8Sheridan Martell9Susanne Middlemiss-Kraak10Pramod Gopal11The New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandRiddet Institute, Massey University, Palmerston North 4442, New ZealandAgResearch Ltd., Grasslands Research Centre, Palmerston North 4442, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandSchool of Food and Advanced Technology, Massey University, Palmerston North 4442, New ZealandAgResearch Ltd., Grasslands Research Centre, Palmerston North 4442, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North 4410, New ZealandThe relationship between the microbiota profile and exposure to stress is not well understood. Therefore, we used a rat model of unpredictable chronic mild stress (UCMS) to investigate this relationship. Depressive-like behaviors were measured in Female Sprague Dawley rats using the sucrose preference test and the Porsolt swim test. Anxiety-like behaviors were measured with the light–dark box test. Fecal corticosterone, cecal microbiota (composition and organic acids), plasma gut permeability (lipopolysaccharide-binding protein, LBP) and plasma inflammation (12 cytokines) markers were measured. Atypical behaviors were observed in female rats following UCMS, but no depressive-like behaviors were observed. Circulating concentrations of cytokines granulocyte-macrophage colony-stimulating factor and cytokine-induced neutrophil chemoattractant 1 were higher in UCMS-exposed female rats; plasma LBP and cecal organic acid levels remained unchanged. Our results reflect a resilient and adaptive phenotype for female SD rats. The relative abundance of taxa from the Clostridiales order and <i>Desulfovibrionaceae</i> family did, however, correlate both positively and negatively with anxiety-like behaviors and plasma cytokine concentrations, regardless of UCMS exposure, supporting the brain-to-gut influence of mild anxiety with a microbiota profile that may involve inflammatory pathways.https://www.mdpi.com/2076-2607/11/7/1773stressanxietymicrobiomecytokinesmicrobiome–gut–brain axisClostridiales
spellingShingle Tracey Bear
Nicole Roy
Julie Dalziel
Chrissie Butts
Jane Coad
Wayne Young
Shanthi G. Parkar
Duncan Hedderley
Hannah Dinnan
Sheridan Martell
Susanne Middlemiss-Kraak
Pramod Gopal
Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal Clostridiales
Microorganisms
stress
anxiety
microbiome
cytokines
microbiome–gut–brain axis
Clostridiales
title Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal Clostridiales
title_full Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal Clostridiales
title_fullStr Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal Clostridiales
title_full_unstemmed Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal Clostridiales
title_short Anxiety-like Behavior in Female Sprague Dawley Rats Associated with Cecal Clostridiales
title_sort anxiety like behavior in female sprague dawley rats associated with cecal clostridiales
topic stress
anxiety
microbiome
cytokines
microbiome–gut–brain axis
Clostridiales
url https://www.mdpi.com/2076-2607/11/7/1773
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