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The gut-brain axis mediates bacterial driven modulation of reward signaling

OBJECTIVE: Our goal is to investigate if microbiota composition modulates reward signaling and assess the role of the vagus in mediating microbiota to brain communication. METHODS: Male germ-free Fisher rats were colonized with gastrointestinal contents from chow (low fat (LF) ConvLF) or HF (ConvHF)...

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Autores principales: Kim, Jiyoung S., Williams, Kevin C., Kirkland, Rebecca A., Schade, Ruth, Freeman, Kimberly G., Cawthon, Carolina R., Rautmann, Allison W., Smith, Jessica M., Edwards, Gaylen L., Glenn, Travis C., Holmes, Philip V., de Lartigue, Guillaume, de La Serre, Claire B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10372379/
https://www.ncbi.nlm.nih.gov/pubmed/37380023
http://dx.doi.org/10.1016/j.molmet.2023.101764
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author Kim, Jiyoung S.
Williams, Kevin C.
Kirkland, Rebecca A.
Schade, Ruth
Freeman, Kimberly G.
Cawthon, Carolina R.
Rautmann, Allison W.
Smith, Jessica M.
Edwards, Gaylen L.
Glenn, Travis C.
Holmes, Philip V.
de Lartigue, Guillaume
de La Serre, Claire B.
author_facet Kim, Jiyoung S.
Williams, Kevin C.
Kirkland, Rebecca A.
Schade, Ruth
Freeman, Kimberly G.
Cawthon, Carolina R.
Rautmann, Allison W.
Smith, Jessica M.
Edwards, Gaylen L.
Glenn, Travis C.
Holmes, Philip V.
de Lartigue, Guillaume
de La Serre, Claire B.
author_sort Kim, Jiyoung S.
collection PubMed
description OBJECTIVE: Our goal is to investigate if microbiota composition modulates reward signaling and assess the role of the vagus in mediating microbiota to brain communication. METHODS: Male germ-free Fisher rats were colonized with gastrointestinal contents from chow (low fat (LF) ConvLF) or HF (ConvHF) fed rats. RESULTS: Following colonization, ConvHF rats consumed significantly more food than ConvLF animals. ConvHF rats displayed lower feeding-induced extracellular DOPAC levels (a metabolite of dopamine) in the Nucleus Accumbens (NAc) as well as reduced motivation for HF foods compared to ConvLF rats. Dopamine receptor 2 (DDR2) expression levels in the NAc were also significantly lower in ConvHF animals. Similar deficits were observed in conventionally raised HF fed rats, showing that diet-driven alteration in reward can be initiated via microbiota. Selective gut to brain deafferentation restored DOPAC levels, DRD2 expression, and motivational drive in ConvHF rats. CONCLUSIONS: We concluded from these data that a HF-type microbiota is sufficient to alter appetitive feeding behavior and that bacteria to reward communication is mediated by the vagus nerve.
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spelling pubmed-103723792023-07-28 The gut-brain axis mediates bacterial driven modulation of reward signaling Kim, Jiyoung S. Williams, Kevin C. Kirkland, Rebecca A. Schade, Ruth Freeman, Kimberly G. Cawthon, Carolina R. Rautmann, Allison W. Smith, Jessica M. Edwards, Gaylen L. Glenn, Travis C. Holmes, Philip V. de Lartigue, Guillaume de La Serre, Claire B. Mol Metab Original Article OBJECTIVE: Our goal is to investigate if microbiota composition modulates reward signaling and assess the role of the vagus in mediating microbiota to brain communication. METHODS: Male germ-free Fisher rats were colonized with gastrointestinal contents from chow (low fat (LF) ConvLF) or HF (ConvHF) fed rats. RESULTS: Following colonization, ConvHF rats consumed significantly more food than ConvLF animals. ConvHF rats displayed lower feeding-induced extracellular DOPAC levels (a metabolite of dopamine) in the Nucleus Accumbens (NAc) as well as reduced motivation for HF foods compared to ConvLF rats. Dopamine receptor 2 (DDR2) expression levels in the NAc were also significantly lower in ConvHF animals. Similar deficits were observed in conventionally raised HF fed rats, showing that diet-driven alteration in reward can be initiated via microbiota. Selective gut to brain deafferentation restored DOPAC levels, DRD2 expression, and motivational drive in ConvHF rats. CONCLUSIONS: We concluded from these data that a HF-type microbiota is sufficient to alter appetitive feeding behavior and that bacteria to reward communication is mediated by the vagus nerve. Elsevier 2023-06-26 /pmc/articles/PMC10372379/ /pubmed/37380023 http://dx.doi.org/10.1016/j.molmet.2023.101764 Text en © 2023 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Original Article
Kim, Jiyoung S.
Williams, Kevin C.
Kirkland, Rebecca A.
Schade, Ruth
Freeman, Kimberly G.
Cawthon, Carolina R.
Rautmann, Allison W.
Smith, Jessica M.
Edwards, Gaylen L.
Glenn, Travis C.
Holmes, Philip V.
de Lartigue, Guillaume
de La Serre, Claire B.
The gut-brain axis mediates bacterial driven modulation of reward signaling
title The gut-brain axis mediates bacterial driven modulation of reward signaling
title_full The gut-brain axis mediates bacterial driven modulation of reward signaling
title_fullStr The gut-brain axis mediates bacterial driven modulation of reward signaling
title_full_unstemmed The gut-brain axis mediates bacterial driven modulation of reward signaling
title_short The gut-brain axis mediates bacterial driven modulation of reward signaling
title_sort gut-brain axis mediates bacterial driven modulation of reward signaling
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10372379/
https://www.ncbi.nlm.nih.gov/pubmed/37380023
http://dx.doi.org/10.1016/j.molmet.2023.101764
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