The central nervous system and the gut microbiome

Sharon, Gil; Sampson, Timothy R.; Geschwind, Daniel H.; Mazmanian, Sarkis K.

doi:10.1016/j.cell.2016.10.027

Cited by 1,513Gut microbiota and healthNeurogenesis and neuroplasticity mechanismsTryptophan and brain disorders

The central nervous system and the gut microbiome

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Sharon, Gil, Sampson, Timothy R., Geschwind, Daniel H., Mazmanian, Sarkis K.·2016·Cell

DOI 10.1016/j.cell.2016.10.027PMC PMC5127403

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Abstract

Summary Neurodevelopment is a complex process governed by both intrinsic and extrinsic signals. While historically studied by researching the brain, inputs from the periphery impact many neurological conditions. Indeed, emerging data suggests communication between the gut and the brain in anxiety, depression, cognition and autism spectrum disorder (ASD). The development of a healthy, functional brain depends on key pre- and post-natal events that integrate environmental cues, such as molecular signals from the gut. These cues largely originate from the microbiome, the consortium of symbiotic bacteria that reside within all animals. Research over the past few years reveals that the gut microbiome plays a role in basic neurogenerative processes such as the formation of the blood-brain-barrier, myelination, neurogenesis, and microglia maturation, and also modulates many aspects of animal behavior. Herein, we discuss the biological intersection of neurodevelopment and the microbiome, and explore the hypothesis that gut bacteria are integral contributors to development and function of the nervous system, and the balance between mental health and disease.

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Delivery mode and early-life occurrences such as feeding changes, infection, and antibiotics treatment have a large effect on gut microbiota composition with a long-term impact on brain and behavior.
“delivery mode (47) and early-life occurrences such as feeding changes, infection, and antibiotics treatment (48, 49) have a huge effect on the gut microbiota composition with a long-term impact on brain and behavior (9, 29).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [29]
In the section “The early life gut microbiome and its impact on brain development and behavior” (page unavailable), the review reports an association between antibiotics in the first year of life and later behavioral difficulties, and describes effects of long-term antibiotic treatment on brain chemistry and behavior. It also says effects on brain development may occur and notes that some short-term antibiotic treatments did not produce lasting behavioral changes. The claim’s unqualified long-term impact is therefore stronger than the source supports. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Modulation of gut physiology by the central nervous system and its effects on gut function such as motility, secretion, blood flow, nociception, and immune function during neurological stressors are well-documented.
“The modulation of gut physiology by the CNS and its effects on gut function such as motility, secretion, blood flow, nociception, and immune function during neurological stressors are well-documented (17, 29, 30).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [29]
The section on the early-life gut microbiome and brain development says brain–gut microbial communication is bidirectional and describes changes in the gut microbiome after early-life stress in mice. It does not document CNS effects on the listed gut functions—motility, secretion, blood flow, nociception, and immune function—during neurological stressors, so the specific claim that these effects are well-documented is not supported by this source. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Short-chain fatty acids that cross into the central nervous system have neuroactive properties.
“Accumulating evidence suggests that SCFAs that cross into the CNS have neuroactive properties.”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [29]
In “Prenatal brain development” (page unavailable), the review reports that administering SCFAs rescues impaired responses of microglia, supporting activity in the CNS. It also reports an effect of butyrate on blood–brain barrier permeability, but does not establish that SCFAs cross into the CNS; that part of the claim is unsupported by our copy. (LLM, conf=0.83)
Experimental — accuracy not yet measured
The microbiota is altered in CNS diseases, which aggravates the condition, and/or its modulation might prevent or improve the development and progression of CNS pathologies.
“The central hypothesis is supported by experimental and clinical evidence that the microbiota is altered in such diseases, which aggravates the condition, and/or its modulation might prevent or improve the development and progression of CNS pathologies (17, 19, 29, 33–37).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [29]
In “The microbiome in neurodegenerative diseases” (page unavailable), the review reports altered gut microbial communities in people with neurodegenerative diseases. It also describes interventions that improve or prevent some conditions, chiefly in animal models. But the Perspective (page unavailable) says it remains unclear whether observed microbial differences cause or aggravate disease, so the claim overstates that part. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Several brain disorders have been linked to imbalances in the microbial composition of the gut.
“several brain disorders have been linked to imbalances in the microbial composition of the gut (17, 19, 29, 33–37)”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [29]

Through SCFAs, the gut microbiota actively communicates with host cells to regulate neurotrophic factors, neurotransmitters, and levels of neuroinflammation by affecting glial cell morphology and function, mitochondrial function, immune activation, lipid metabolism, and gene expression, thereby influencing central nervous system functions.
“Through SCFAs, the gut microbiota actively communicates with host cells to regulate neurotrophic factors, neurotransmitters, and levels of neuroinflammation by affecting glial cell morphology and function, mitochondrial function, immune activation, lipid metabolism, and gene expression, thereby influencing CNS functions.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [54]
The maturation and function of CNS-resident macrophages and microglia are controlled by the gut microbiota.
“The maturation and function of CNS-resident macrophages and microglia are controlled by the gut microbiota (54).”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [54]
Animal studies suggest that the GM plays a crucial role in regulating early brain development.
“Animal studies suggest that the GM plays a crucial role in regulating early brain development (19, 45, 60, 114–117).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [116]
Altered SCFA production is demonstrated in a variety of neuropathologies.
“Altered SCFA production has also been demonstrated in a variety of neuropathologies (42, 116, 127, 130, 132, 292–295).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [116]
A large body of preclinical literature supports the notion of a bidirectional communication system linking the gut and the brain, known as the gut-microbiota-brain axis.
“A large body of preclinical literature supports the notion of a bidirectional communication system linking the gut and the brain, known as the gut-microbiota-brain axis (Borre et al., 2014; Sharon et al., 2016; Vuong et al., 2017).”
From Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder (2019) · cites this paper as Sharon et al., 2016

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THE DEVELOPMENT OF THE HUMAN BLOOD‐BRAIN AND BLOOD‐CSF BARRIERS
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The human intestinal microbiome at extreme ages of life. Dietary intervention as a way to counteract alterations
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“Others have reported that antibiotic administration during the first year of life was correlated with depression and behavioral difficulties later in life (Slykerman et al., 2016).”
Background
Functional Dynamics of the Gut Microbiome in Elderly People during Probiotic Consumption
Eloe-Fadrosh, E. A., Brady, A., Crabtree, J., Drabek, E. F., Ma, B., Mahurkar, A., Ravel, J., Haverkamp, M., Fiorino, A.-M., Botelho, C., et al. (2015) · mBio · doi:10.1128/mbio.00231-15 · Cited by 160 · see citing works
Administration of Non-Absorbable Antibiotics to Pregnant Mice to Perturb the Maternal Gut Microbiota Is Associated with Alterations in Offspring Behavior
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A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment
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Clostridium butyricum attenuates cerebral ischemia/reperfusion injury in diabetic mice via modulation of gut microbiota
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Aging and Intestinal Motility
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Pre- and Neonatal Exposure to Lipopolysaccharide or the Enteric Metabolite, Propionic Acid, Alters Development and Behavior in Adolescent Rats in a Sexually Dimorphic Manner
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Minocycline treatment ameliorates interferon-alpha- induced neurogenic defects and depression-like behaviors in mice
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Metagenomic Sequencing Indicates That the Oropharyngeal Phageome of Individuals With Schizophrenia Differs From That of Controls
Yolken, R. H., Severance, E. G., Sabunciyan, S., Gressitt, K. L., Chen, O., Stallings, C. R., Origoni, A. E., Katsafanas, E., Schweinfurth, L. A. B., Savage, C. L. G., et al. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu197 · Cited by 123 · see citing works
Erratum to: The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women
Romero, R. J., Hassan, S. S., Gajer, P., Tarca, A. L., Fadrosh, D. W., Nikita, L., Galuppi, M., Lamont, R., Chaemsaithong, P., Miranda, J., et al. (2014) · Microbiome · doi:10.1186/2049-2618-2-10 · Cited by 120 · see citing works
Antidepressant-like actions of minocycline combined with several glutamate antagonists
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Does Maternal Perinatal Probiotic Supplementation Alter the Intestinal Microbiota of Mother and Child?
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Ageing and the gut
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Neurotrophins and cell death
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Maternal gut and fetal brain connection: Increased anxiety and reduced social interactions in Wistar rat offspring following peri-conceptional antibiotic exposure
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Immunity and inflammation in neurodegenerative diseases.
Cappellano, G., Carecchio, M., Fleetwood, T., Magistrelli, L., Cantello, R. M., Dianzani, U., & Comi, C. (2013) · Europe PMC (PubMed Central) · Cited by 105 · see citing works
Transcriptome analysis in whole blood reveals increased microbial diversity in schizophrenia
Loohuis, L. M. O., Mangul, S., Ori, A. P. S., Jospin, G., Koslicki, D., Yang, H. T., Wu, T., Boks, M. P., Lomen‐Hoerth, C., Wiedau‐Pazos, M., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0107-9 · Cited by 104 · see citing works
Bacterial peptidoglycan traverses the placenta to induce fetal neuroproliferation and aberrant postnatal behavior
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Microglia: Phagocytosing to Clear, Sculpt, and Eliminate
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Comparison of Brain Maturation among Species: An Example in Translational Research Suggesting the Possible Use of Bumetanide in Newborn
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Neurotrophins in the Regulation of Cellular Survival and Death
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Changes in Intestinal Glucocorticoid Sensitivity in Early Life Shape the Risk of Epithelial Barrier Defect in Maternal-Deprived Rats
Moussaoui, N., Braniste, V., Ait-Belgnaoui, A., Gabanou, M., Sekkal, S., Olier, M., Théodorou, V., Martin, P. G. P., & Houdeau, É. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088382 · Cited by 83 · see citing works
Food allergy and food‐based therapies in neurodevelopmental disorders
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Abnormal Lipopolysaccharide Binding Protein as Marker of Gastrointestinal Inflammation in Parkinson Disease
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Fecal microbiota transplantation in children: a brief review
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Bacterial Peptidoglycan Traverses the Placenta to Induce Fetal Neuroproliferation and Aberrant Postnatal Behavior
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Title: Reduction of Alzheimer's disease beta-amyloid pathology in the absence of gut microbiotaPreprint
Harach, T., Marungruang, N., Dutilleul, N., Cheatham, V., Coy, K. D. M., Neher, J. J., Jucker, M., Fåk, F., Lasser, & Bolmont, T. (2015) · arXiv (Cornell University) · Cited by 21 · see citing works
Digestive Symptoms in Older Adults: Prevalence and Associations with Institutionalization and Mortality
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Transcriptome analysis in whole blood reveals increased microbial diversity in schizophreniaPreprint
Loohuis, L. M. O., Mangul, S., Ori, A. P. S., et al. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/057570 · Cited by 15 · see citing works

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Interaction between microbiota and immunity in health and disease
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Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease
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The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication
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Sodium oligomannate therapeutically remodels gut microbiota and suppresses gut bacterial amino acids-shaped neuroinflammation to inhibit Alzheimer’s disease progression
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Chemical transformation of xenobiotics by the human gut microbiota
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Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder
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The Gut Microbiota and Alzheimer’s Disease
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Microbiota-Brain-Gut Axis and Neurodegenerative Diseases
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Microbiome Influences Prenatal and Adult Microglia in a Sex-Specific Manner
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Discovery and inhibition of an interspecies gut bacterial pathway for Levodopa metabolism
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Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota
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A Neural Circuit for Gut-Induced Reward
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The gut microbiome from patients with schizophrenia modulates the glutamate-glutamine-GABA cycle and schizophrenia-relevant behaviors in mice
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Potential roles of gut microbiome and metabolites in modulating ALS in mice
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Microbial tryptophan metabolites regulate gut barrier function via the aryl hydrocarbon receptor
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Altered Microbiomes Distinguish Alzheimer’s Disease from Amnestic Mild Cognitive Impairment and Health in a Chinese Cohort
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Our gut microbiome: The evolving inner self
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Regulation of inflammation by microbiota interactions with the host
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Zebrafish as an animal model for biomedical research
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A Comprehensive Review on the Role of the Gut Microbiome in Human Neurological Disorders
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Probiotic Supplementation Improves Cognitive Function and Mood with Changes in Gut Microbiota in Community-Dwelling Older Adults: A Randomized, Double-Blind, Placebo-Controlled, Multicenter Trial
Kim, C.-S., Cha, J., Sim, M., Jung, S., Chun, W. Y., Baik, H. W., & Shin, D.-M. (2020) · The Journals of Gerontology Series A · doi:10.1093/gerona/glaa090 · Cited by 551 · see citing works
Functions of Gut Microbiota Metabolites, Current Status and Future Perspectives
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A gut-derived metabolite alters brain activity and anxiety behaviour in mice
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Host–microbiota interactions in immune-mediated diseases
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Gut Bacteria and Neurotransmitters
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Mild cognitive impairment has similar alterations as Alzheimer's disease in gut microbiota
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Role of gut-brain axis, gut microbial composition, and probiotic intervention in Alzheimer's disease
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Microbiota-gut-brain axis: Modulator of host metabolism and appetite
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Dysbiosis of gut microbiota and microbial metabolites in Parkinson's disease
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Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health
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Altered Gut Microbiota in a Mouse Model of Alzheimer’s Disease
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Age‐related changes in the gut microbiota influence systemic inflammation and stroke outcome
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Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
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Authors: Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K.
Affiliations: California Institute of Technology (US)
University of California, Los Angeles (US)
Corresponding author: Sharon, Gil
Mazmanian, Sarkis K.
ORCID: Sharon, Gil
Sampson, Timothy R.
Geschwind, Daniel H.
Mazmanian, Sarkis K.
Venue: Cell
Publisher: Elsevier BV
Published: 2016-11
Volume: 167
Issue: 4
Pages: 915-932
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2016.10.027
PMC: PMC5127403
OpenAlex: W2548933161
Semantic Scholar: 7bb11be31e7f534cb591760aeb939cd84b4b45ac
Cited by: 1,513
References: 190
Citations by year: 2026: 140 · 2025: 157 · 2024: 198 · 2023: 186 · 2022: 175 · 2021: 211 · 2020: 160 · 2019: 128 · 2018: 95 · 2017: 60 · 2016: 2
FWCI: 8.63
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 367 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
CaltechAUTHORS (California Institute of Technology) (submittedVersion)
Funders: Meixner Postdoctoral Fellowship in Translational Research
Larry L. Hillblom Foundation Postdoctoral Fellowship
NIH (MH100556, DK078938, GM099535, NS085910)
Department of Defense
Heritage Medical Research Institute
Simons Foundation
NIMH (HD055784, MH100027, MH110927, MH1064382)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: gut microbiota, central nervous system, brain development, gut-brain axis, anxiety, depression, autism spectrum disorder, blood-brain barrier, myelination, neurogenesis, behavior, mental health
MeSH terms: Gastrointestinal Microbiome, Animals, Behavior, Brain, Female, Humans, Pregnancy, Vagina, Neurodevelopmental Disorders

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