Cargando…

Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development

Growing evidence is demonstrating the connection between the microbiota gut-brain axis and neurodevelopment. Microbiota colonization occurs before the maturation of many neural systems and is linked to brain health. Because of this it has been hypothesized that the early microbiome interactions alon...

Descripción completa

Detalles Bibliográficos
Autores principales: Hunter, Sebastian, Flaten, Erica, Petersen, Charisse, Gervain, Judit, Werker, Janet F., Trainor, Laurel J., Finlay, Brett B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10411758/
https://www.ncbi.nlm.nih.gov/pubmed/37556397
http://dx.doi.org/10.1371/journal.pone.0288689
_version_ 1785086738989842432
author Hunter, Sebastian
Flaten, Erica
Petersen, Charisse
Gervain, Judit
Werker, Janet F.
Trainor, Laurel J.
Finlay, Brett B.
author_facet Hunter, Sebastian
Flaten, Erica
Petersen, Charisse
Gervain, Judit
Werker, Janet F.
Trainor, Laurel J.
Finlay, Brett B.
author_sort Hunter, Sebastian
collection PubMed
description Growing evidence is demonstrating the connection between the microbiota gut-brain axis and neurodevelopment. Microbiota colonization occurs before the maturation of many neural systems and is linked to brain health. Because of this it has been hypothesized that the early microbiome interactions along the gut-brain axis evolved to promote advanced cognitive functions and behaviors. Here, we performed a pilot study with a multidisciplinary approach to test if the microbiota composition of infants is associated with measures of early cognitive development, in particular neural rhythm tracking; language (forward speech) versus non-language (backwards speech) discrimination; and social joint attention. Fecal samples were collected from 56 infants between four and six months of age and sequenced by shotgun metagenomic sequencing. Of these, 44 performed the behavioral Point and Gaze test to measure joint attention. Infants were tested on either language discrimination using functional near-infrared spectroscopy (fNIRS; 25 infants had usable data) or neural rhythm tracking using electroencephalogram (EEG; 15 had usable data). Infants who succeeded at the Point and Gaze test tended to have increased Actinobacteria and reduced Firmicutes at the phylum level; and an increase in Bifidobacterium and Eggerthella along with a reduction in Hungatella and Streptococcus at the genus level. Measurements of neural rhythm tracking associated negatively to the abundance of Bifidobacterium and positively to the abundance of Clostridium and Enterococcus for the bacterial abundances, and associated positively to metabolic pathways that can influence neurodevelopment, including branched chain amino acid biosynthesis and pentose phosphate pathways. No associations were found for the fNIRS language discrimination measurements. Although the tests were underpowered due to the small pilot sample sizes, potential associations were identified between the microbiome and measurements of early cognitive development that are worth exploring further.
format Online
Article
Text
id pubmed-10411758
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-104117582023-08-10 Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development Hunter, Sebastian Flaten, Erica Petersen, Charisse Gervain, Judit Werker, Janet F. Trainor, Laurel J. Finlay, Brett B. PLoS One Research Article Growing evidence is demonstrating the connection between the microbiota gut-brain axis and neurodevelopment. Microbiota colonization occurs before the maturation of many neural systems and is linked to brain health. Because of this it has been hypothesized that the early microbiome interactions along the gut-brain axis evolved to promote advanced cognitive functions and behaviors. Here, we performed a pilot study with a multidisciplinary approach to test if the microbiota composition of infants is associated with measures of early cognitive development, in particular neural rhythm tracking; language (forward speech) versus non-language (backwards speech) discrimination; and social joint attention. Fecal samples were collected from 56 infants between four and six months of age and sequenced by shotgun metagenomic sequencing. Of these, 44 performed the behavioral Point and Gaze test to measure joint attention. Infants were tested on either language discrimination using functional near-infrared spectroscopy (fNIRS; 25 infants had usable data) or neural rhythm tracking using electroencephalogram (EEG; 15 had usable data). Infants who succeeded at the Point and Gaze test tended to have increased Actinobacteria and reduced Firmicutes at the phylum level; and an increase in Bifidobacterium and Eggerthella along with a reduction in Hungatella and Streptococcus at the genus level. Measurements of neural rhythm tracking associated negatively to the abundance of Bifidobacterium and positively to the abundance of Clostridium and Enterococcus for the bacterial abundances, and associated positively to metabolic pathways that can influence neurodevelopment, including branched chain amino acid biosynthesis and pentose phosphate pathways. No associations were found for the fNIRS language discrimination measurements. Although the tests were underpowered due to the small pilot sample sizes, potential associations were identified between the microbiome and measurements of early cognitive development that are worth exploring further. Public Library of Science 2023-08-09 /pmc/articles/PMC10411758/ /pubmed/37556397 http://dx.doi.org/10.1371/journal.pone.0288689 Text en © 2023 Hunter et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hunter, Sebastian
Flaten, Erica
Petersen, Charisse
Gervain, Judit
Werker, Janet F.
Trainor, Laurel J.
Finlay, Brett B.
Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development
title Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development
title_full Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development
title_fullStr Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development
title_full_unstemmed Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development
title_short Babies, bugs and brains: How the early microbiome associates with infant brain and behavior development
title_sort babies, bugs and brains: how the early microbiome associates with infant brain and behavior development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10411758/
https://www.ncbi.nlm.nih.gov/pubmed/37556397
http://dx.doi.org/10.1371/journal.pone.0288689
work_keys_str_mv AT huntersebastian babiesbugsandbrainshowtheearlymicrobiomeassociateswithinfantbrainandbehaviordevelopment
AT flatenerica babiesbugsandbrainshowtheearlymicrobiomeassociateswithinfantbrainandbehaviordevelopment
AT petersencharisse babiesbugsandbrainshowtheearlymicrobiomeassociateswithinfantbrainandbehaviordevelopment
AT gervainjudit babiesbugsandbrainshowtheearlymicrobiomeassociateswithinfantbrainandbehaviordevelopment
AT werkerjanetf babiesbugsandbrainshowtheearlymicrobiomeassociateswithinfantbrainandbehaviordevelopment
AT trainorlaurelj babiesbugsandbrainshowtheearlymicrobiomeassociateswithinfantbrainandbehaviordevelopment
AT finlaybrettb babiesbugsandbrainshowtheearlymicrobiomeassociateswithinfantbrainandbehaviordevelopment