Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects

A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota...

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Published inPloS one Vol. 13; no. 8; p. e0201772
Main Authors Osadchiy, Vadim, Labus, Jennifer S., Gupta, Arpana, Jacobs, Jonathan, Ashe-McNalley, Cody, Hsiao, Elaine Y., Mayer, Emeran A.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 06.08.2018
Public Library of Science (PLoS)
Subjects
Addictions
Adolescent
Adult
Amygdala
Anxiety
Behavior, Addictive - diagnostic imaging
Behavior, Addictive - metabolism
Biology and Life Sciences
Body mass
Body Mass Index
Body size
Brain
Brain - diagnostic imaging
Brain - metabolism
Brain mapping
Computer and Information Sciences
Cross-Sectional Studies
Diffusion Tensor Imaging
Eating behavior
Enzymes
Fecal microflora
Feces - microbiology
Feeding Behavior - physiology
Female
Females
Food
Food intake
Functional magnetic resonance imaging
Gastrointestinal Microbiome - physiology
Gene expression
Graph theory
Health aspects
Healthy Volunteers
Humans
Hydrocarbons
Indoleacetic acid
Indoles - metabolism
Intestinal microflora
Ligands
Magnetic Resonance Imaging
Male
Males
Medicine and Health Sciences
Metabolism
Metabolites
Microbiota
Middle Aged
Network analysis
Neural networks
Neural Pathways - diagnostic imaging
Neural Pathways - metabolism
Neurobiology
Neuroimaging
Neurosciences
Nucleus accumbens
Obesity
Obesity - diagnostic imaging
Obesity - metabolism
Physical Sciences
Physiology
Reinforcement
Reward
Social Sciences
Tryptophan
Tryptophan - metabolism
Young Adult
Los Angeles California
United States > US
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Abstract A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain's extended reward network and clinical measures related to obesity. DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded. The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety). The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.
AbstractList Objective A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain’s extended reward network and clinical measures related to obesity. Methods DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded. Results The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety). Conclusions The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.
Objective A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain’s extended reward network and clinical measures related to obesity. Methods DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded. Results The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety). Conclusions The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.
A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain's extended reward network and clinical measures related to obesity. DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded. The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety). The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.
A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain's extended reward network and clinical measures related to obesity. DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded. The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety). The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.
A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain's extended reward network and clinical measures related to obesity.OBJECTIVEA growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and disease, including hedonic food intake and obesity. We performed a tripartite network analysis based on graph theory to test the hypothesis that microbiota-derived fecal metabolites are associated with connectivity of key regions of the brain's extended reward network and clinical measures related to obesity.DTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded.METHODSDTI and resting state fMRI imaging was obtained from 63 healthy subjects with and without elevated body mass index (BMI) (29 males and 34 females). Subjects submitted fecal samples, completed questionnaires to assess anxiety and food addiction, and BMI was recorded.The study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety).RESULTSThe study results demonstrate associations between fecal microbiota-derived indole metabolites (indole, indoleacetic acid, and skatole) with measures of functional and anatomical connectivity of the amygdala, nucleus accumbens, and anterior insula, in addition to BMI, food addiction scores (YFAS) and anxiety symptom scores (HAD Anxiety).The findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.CONCLUSIONSThe findings support the hypothesis that gut microbiota-derived indole metabolites may influence hedonic food intake and obesity by acting on the extended reward network, specifically the amygdala-nucleus accumbens circuit and the amygdala-anterior insula circuit. These cross sectional, data-driven results provide valuable information for future mechanistic studies.
Audience Academic
Author Ashe-McNalley, Cody
Hsiao, Elaine Y.
Osadchiy, Vadim
Labus, Jennifer S.
Gupta, Arpana
Jacobs, Jonathan
Mayer, Emeran A.
AuthorAffiliation Instituto de Agroquimica y Tecnologia de Alimentos, SPAIN
1 G. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, Los Angeles, CA, United States of America
3 UCLA Department of Integrative Biology and Physiology, Los Angeles, CA, United States of America
2 UCLA Microbiome Center, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America
AuthorAffiliation_xml – name: 2 UCLA Microbiome Center, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America
– name: 3 UCLA Department of Integrative Biology and Physiology, Los Angeles, CA, United States of America
– name: Instituto de Agroquimica y Tecnologia de Alimentos, SPAIN
– name: 1 G. Oppenheimer Center for Neurobiology of Stress and Resilience, UCLA Vatche and Tamar Manoukian Division of Digestive Diseases, Los Angeles, CA, United States of America
Author_xml – sequence: 1
  givenname: Vadim
  surname: Osadchiy
  fullname: Osadchiy, Vadim
– sequence: 2
  givenname: Jennifer S.
  surname: Labus
  fullname: Labus, Jennifer S.
– sequence: 3
  givenname: Arpana
  surname: Gupta
  fullname: Gupta, Arpana
– sequence: 4
  givenname: Jonathan
  surname: Jacobs
  fullname: Jacobs, Jonathan
– sequence: 5
  givenname: Cody
  surname: Ashe-McNalley
  fullname: Ashe-McNalley, Cody
– sequence: 6
  givenname: Elaine Y.
  surname: Hsiao
  fullname: Hsiao, Elaine Y.
– sequence: 7
  givenname: Emeran A.
  orcidid: 0000-0003-3923-3349
  surname: Mayer
  fullname: Mayer, Emeran A.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30080865$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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2018 Osadchiy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Competing Interests: EAM is a scientific advisory board member of Danone, Danone Northamerica, Axial Biotherapeutics, Viome, Amare, Pharmavite and Prolacta. None of these companies were in any way involved in the current study, and this board membership does not alter the adherence of the authors to PLOS ONE policies on sharing data and materials.
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Objective A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and...
OBJECTIVE:A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and...
Objective A growing body of preclinical and clinical literature suggests that brain-gut-microbiota interactions play an important role in human health and...
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SubjectTerms Addictions
Adolescent
Adult
Amygdala
Anxiety
Behavior, Addictive - diagnostic imaging
Behavior, Addictive - metabolism
Biology and Life Sciences
Body mass
Body Mass Index
Body size
Brain
Brain - diagnostic imaging
Brain - metabolism
Brain mapping
Computer and Information Sciences
Cross-Sectional Studies
Diffusion Tensor Imaging
Eating behavior
Enzymes
Fecal microflora
Feces - microbiology
Feeding Behavior - physiology
Female
Females
Food
Food intake
Functional magnetic resonance imaging
Gastrointestinal Microbiome - physiology
Gene expression
Graph theory
Health aspects
Healthy Volunteers
Humans
Hydrocarbons
Indoleacetic acid
Indoles - metabolism
Intestinal microflora
Ligands
Magnetic Resonance Imaging
Male
Males
Medicine and Health Sciences
Metabolism
Metabolites
Microbiota
Middle Aged
Network analysis
Neural networks
Neural Pathways - diagnostic imaging
Neural Pathways - metabolism
Neurobiology
Neuroimaging
Neurosciences
Nucleus accumbens
Obesity
Obesity - diagnostic imaging
Obesity - metabolism
Physical Sciences
Physiology
Reinforcement
Reward
Social Sciences
Tryptophan
Tryptophan - metabolism
Young Adult
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Title Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects
URI https://www.ncbi.nlm.nih.gov/pubmed/30080865
https://www.proquest.com/docview/2084328022
https://www.proquest.com/docview/2084919913
https://pubmed.ncbi.nlm.nih.gov/PMC6078307
https://doaj.org/article/a18b15ec3f804ad193d994ed84928ca7
http://dx.doi.org/10.1371/journal.pone.0201772
Volume 13
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