Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats
Abstract
Disruption of bacterial colonization during the early postnatal period is increasingly being linked to adverse health outcomes. Indeed, there is a growing appreciation that the gut microbiota plays a role in neurodevelopment. However, there is a paucity of information on the consequences of early-life manipulations of the gut microbiota on behavior. To this end we administered an antibiotic (vancomycin) from postnatal days 4-13 to male rat pups and assessed behavioral and physiological measures across all aspects of the brain-gut axis. In addition, we sought to confirm and expand the effects of early-life antibiotic treatment using a different antibiotic strategy (a cocktail of pimaricin, bacitracin, neomycin; orally) during the same time period in both female and male rat pups. Vancomycin significantly altered the microbiota, which was restored to control levels by 8 weeks of age. Notably, vancomycin-treated animals displayed visceral hypersensitivity in adulthood without any significant effect on anxiety responses as assessed in the elevated plus maze or open field tests. Moreover, cognitive performance in the Morris water maze was not affected by early-life dysbiosis. Immune and stress-related physiological responses were equally unaffected. The early-life antibiotic-induced visceral hypersensitivity was also observed in male rats given the antibiotic cocktail. Both treatments did not alter visceral pain perception in female rats. Changes in visceral pain perception in males were paralleled by distinct decreases in the transient receptor potential cation channel subfamily V member 1, the α-2A adrenergic receptor and cholecystokinin B receptor. In conclusion, a temporary disruption of the gut microbiota in early-life results in very specific and long-lasting changes in visceral sensitivity in male rats, a hallmark of stress-related functional disorders of the brain-gut axis such as irritable bowel disorder.
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Chronic antibiotic treatment impaired spatial memory in the Morris Water Maze in adult rats, while acute treatments did not affect this type of memory when administered in early life in rats or during adulthood in mice tested in the Barnes maze.
“While chronic antibiotic treatment impaired spatial memory in the Morris Water Maze in adult rats (Hoban et al., 2016a;Wang et al., 2015) acute treatments did not affect this type of memory when administered in early life in rats (O'Mahony et al., 2014), nor when administered during adulthood in mice and tested in the Barnes maze (Frohlich et al., 2016).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as O'Mahony et al., 2014
Disruption of the gut microbiota in early life is associated with long-term changes in visceral sensitivity, emphasizing the importance of the gut microbiome in neurodevelopment of pain pathways.
“Disruption of the gut microbiota in early-life also has been associated with longterm changes in visceral sensitivity, emphasizing the importance of the gut microbiome in neurodevelopment of pain pathways68.”
From The gut Microbiome in adult and pediatric functional gastrointestinal disorders (2019) · cites this paper as [68]
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Self-citationStress & the gut-brain axis: Regulation by the microbiome
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Self-citationFrom gut dysbiosis to altered brain function and mental illness: mechanisms and pathways
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Self-citationKynurenine pathway metabolism and the microbiota-gut-brain axis
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Self-citationThe microbiome and host behavior
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The microbiome: a key regulator of stress and neuroinflammation
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Self-citationInfluence of high-fat diet on gut microbiota
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Gut microbiota and the neuroendocrine system
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Pain regulation by gut microbiota: molecular mechanisms and therapeutic potential
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Stress and the Microbiota–Gut–Brain Axis in Visceral Pain: Relevance to Irritable Bowel Syndrome
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Self-citationIntestinal microbiota shapes gut physiology and regulates enteric neurons and glia
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Glutamatergic Signaling Along The Microbiota-Gut-Brain Axis
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Depression's Unholy Trinity: Dysregulated Stress, Immunity, and the Microbiome
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Self-citationMicrobiota-gut-brain axis and the central nervous system
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Self-citationSex differences in the gut microbiome–brain axis across the lifespan
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Self-citationThe Microbiome in Psychology and Cognitive Neuroscience
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Self-citationAltered microbiome composition in individuals with fibromyalgia
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Intestinal microbiota in early life and its implications on childhood health
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Microbiota-gut-brain signalling in Parkinson's disease: Implications for non-motor symptoms
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Self-citationYou’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Self-citationEarly-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
O’Mahony, S. M., Clarke, G., Dinan, T. G., & Cryan, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.068 · Cited by 203 · see citing works
Self-citationProgramming Bugs: Microbiota and the Developmental Origins of Brain Health and Disease
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Priming for Life: Early Life Nutrition and the Microbiota-Gut-Brain Axis
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Self-citationCowan, C. S. M., Dinan, T. G., & Cryan, J. F. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13156 · Cited by 176 · see citing works
Self-citationKey role of gut microbiota in anhedonia-like phenotype in rodents with neuropathic pain
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Microbiota regulates visceral pain in the mouse
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The gut Microbiome in adult and pediatric functional gastrointestinal disorders
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The infant gut microbiome as a microbial organ influencing host well-being
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Self-citationMoody microbes or fecal phrenology: what do we know about the microbiota-gut-brain axis?
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Self-citationImpact of Microbial Metabolites on Microbiota–Gut–Brain Axis in Inflammatory Bowel Disease
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Gut-Brain-Microbiota Axis: Antibiotics and Functional Gastrointestinal Disorders
Karakan, T., Özkul, C., Akkol, E. K., Bilici, S., Sobarzo‐Sánchez, E., & Capasso, R. (2021) · Nutrients · doi:10.3390/nu13020389 · Cited by 155 · see citing works
Jašarević, E., Rodgers, A. B., & Bale, T. L. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.005 · Cited by 147 · see citing works
Diet, gut microbiota and cognition
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Influence of the microbiota-gut-brain axis on behavior and welfare in farm animals: A review
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Gut Microbiota: A Perspective for Psychiatrists
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Self-citationAit-Belgnaoui, A., Payard, I., Rolland, C., Harkat, C., Braniste, V., Théodorou, V., & Tompkins, T. A. (2018) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16167 · Cited by 139 · see citing works
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Microbial colonization is required for normal neurobehavioral development in zebrafish
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The Gut-Microglia Connection: Implications for Central Nervous System Diseases
Wang, Y., Wang, Z., Wang, Y., Li, F., Jia, J., Song, X., Qin, S., Wang, R., Jin, F., Kitazato, K., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02325 · Cited by 128 · see citing works
More than a gut feeling: the microbiota regulates neurodevelopment and behavior
Cryan, J. F., & Dinan, T. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.224 · Cited by 124 · see citing works
Self-citationThe Mycobiome: A Neglected Component in the Microbiota-Gut-Brain Axis
Enaud, R., Vandenborght, L., Coron, N., Bazin, T., Prével, R., Schaeverbeke, T., Berger, P., Fayon, M. J., Lamireau, T., & Delhaès, L. (2018) · Microorganisms · doi:10.3390/microorganisms6010022 · Cited by 116 · see citing works
Depressed gut? The microbiota-diet-inflammation trialogue in depression
Koopman, M., & El Aidy, S. (2017) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000350 · Cited by 114 · see citing works
Altered gut microbiota and endocannabinoid system tone in vitamin D deficiency-mediated chronic pain
Guida, F., Boccella, S., Belardo, C., Iannotta, M., Piscitelli, F., Filippis, F. D., Paino, S., Ricciardi, F., Siniscalco, D., Marabese, I., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.04.006 · Cited by 111 · see citing works
Impact of prebiotics on metabolic and behavioral alterations in a mouse model of metabolic syndrome
de Cossío, L. F., Fourrier, C., Sauvant, J., Everard, A., Capuron, L., Cani, P. D., Layé, S., & Castanon, N. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.12.022 · Cited by 108 · see citing works
Gutsy Moves: The Amygdala as a Critical Node in Microbiota to Brain Signaling
Cowan, C. S. M., Hoban, A. E., Ventura‐Silva, A. P., Dinan, T. G., Clarke, G. A., & Cryan, J. F. (2017) · BioEssays · doi:10.1002/bies.201700172 · Cited by 107 · see citing works
Self-citationEarly exposure to antibiotic drugs and risk for psychiatric disorders: a population-based study
Lavebratt, C., Yang, L. L., Giacobini, M., Forsell, Y., Schalling, M., Partonen, T., & Gissler, M. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0653-9 · Cited by 104 · see citing works
Visceral pain: gut microbiota, a new hope?
Pusceddu, M. M., & Gareau, M. G. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0476-7 · Cited by 100 · see citing works
Degroote, S., Hunting, D. J., Baccarelli, A. A., & Takser, L. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.06.010 · Cited by 106 · see citing works
The gut microbiota as a key regulator of visceral pain
O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2016) · Pain · doi:10.1097/j.pain.0000000000000779 · Cited by 98 · see citing works
Self-citationNeufeld, K. M., O’Mahony, S. M., Hoban, A. E., Waworuntu, R. V., Berg, B. M., Dinan, T. G., & Cryan, J. F. (2017) · Nutritional Neuroscience · doi:10.1080/1028415x.2017.1397875 · Cited by 98 · see citing works
Self-citationMicrobiome: Bacterial broadband
Eisenstein, M. (2016) · Nature · doi:10.1038/533s104a · Cited by 95 · see citing works
Gut Microbiota: A Modulator of Brain Plasticity and Cognitive Function in Ageing
Leung, K., & Thuret, S. (2015) · Healthcare · doi:10.3390/healthcare3040898 · Cited by 92 · see citing works
Targeting the gut microbiota to influence brain development and function in early life
Wang, S., Harvey, L., Martı́n, R., van der Beek, E. M., Knol, J., Cryan, J. F., & Renes, I. B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.002 · Cited by 92 · see citing works
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The Microbiota–Gut–Brain Axis and Neurological Disorders: A Comprehensive Review
Nakhal, M. M., Yassin, L. K., Alyaqoubi, R., Saeed, S., Alderei, A., Alhammadi, A., Alshehhi, M., Almehairbi, A., Houqani, S. A., BaniYas, S., et al. (2024) · Life · doi:10.3390/life14101234 · Cited by 134 · see citing works
Alcohol, microbiome, and their effect on psychiatric disorders
Hillemacher, T., Bachmann, O. P., Kahl, K. G., & Frieling, H. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.04.015 · Cited by 87 · see citing works
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Gut-brain axis: A matter of concern in neuropsychiatric disorders…!
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- Authors
- O’Mahony, S. M., Felice, V. D., Nally, K., Savignac, H. M., Claesson, M. J., Scully, P., Woznicki, J., Hyland, N. P., Shanahan, F., Quigley, E. M., Marchesi, J. R., O’Toole, P. W., Dinan, T. G., & Cryan, J. F.
- Affiliations
- University College Cork (IE)
- ORCID
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2014-09
- Volume
- 277
- Pages
- 885-901
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2055122111
- Cited by
- 272
- References
- 106
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 24 · 2023: 15 · 2022: 18 · 2021: 42 · 2020: 24 · 2019: 26 · 2018: 23 · 2017: 25 · 2016: 34 · 2015: 16 · 2014: 5
- FWCI
- 10.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- Science Foundation Ireland (02/CE/B124, 07/CE/B1368)
- GlaxoSmithKline
- European Community’s Seventh Framework Programme (FP7/2007-2013)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Keywords
- gut microbiota, early-life antibiotic exposure, vancomycin, visceral hypersensitivity, visceral pain, gut-brain axis, brain development, anxiety-like behavior, cognitive performance, sex differences, TRPV1, alpha2A-adrenergic receptor, cholecystokinin B receptor, irritable bowel syndrome
- MeSH terms
- Animals, Animals, Newborn, Anti-Bacterial Agents, Anxiety, Bacitracin, Behavior, Animal, Cognition, Female, Hyperalgesia, Male, Neomycin, Natamycin, Vancomycin, Rats, Sprague-Dawley, Gastrointestinal Tract, Visceral Pain, Microbiota
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