Microbes & neurodevelopment – Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala
Abstract
The mammalian amygdala is a key emotional brain region for eliciting social behaviour, critically involved in anxiety and fear-related behaviours, and hence a focus of research on neurodevelopmental and stress-related disorders such as autism and anxiety. Recently, increasing evidence implicates host-microbe interactions in the aetiology of these conditions. Germ-free (GF) mice, devoid of any microbiota throughout organismal maturation, are a well-established tool to study the effects of absence of the microbiota on host physiology. A growing body of independently replicated findings confirm that GF animals demonstrate altered anxiety-related behaviour and impaired social behaviour. However, the underlying mechanisms of this interaction and the nature of the pathways involved are only insufficiently understood. To further elucidate the molecular underpinnings of microbe-brain interaction, we therefore exploited unbiased genome-wide transcriptional profiling to determine gene expression in the amygdala of GF and GF mice that have been colonised after weaning. Using RNA-sequencing and a comprehensive downstream analysis pipeline we studied the amygdala transcriptome and found significant differences at the levels of differential gene expression, exon usage and RNA-editing. Most surprisingly, we noticed upregulation of several immediate early response genes such as Fos, Fosb, Egr2 or Nr4a1 in association with increased CREB signalling in GF mice. In addition, we found differential expression and recoding of several genes implicated in brain physiology processes such as neurotransmission, neuronal plasticity, metabolism and morphology. In conclusion, our data suggest altered baseline neuronal activity in the amygdala of germ-free animals, which is established during early life and may have implications for understanding development and treatment of neurodevelopmental disorders.
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Gut microbes not only regulate gene expression in the mouse brain, but also affect alternative splicing, and can regulate the production of specific isoforms of genes that have been implicated in ASD.
“These findings suggest that gut microbes not only regulate gene expression in the mouse brain (Hoban et al., 2016; Neufeld et al., 2011; Stilling et al., 2015), but also affect alternative splicing (Stilling et al., 2018), and can regulate the production of specific isoforms of genes that have been implicated in ASD.”
From Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice (2019) · cites this paper as Stilling et al., 2015
Gut microbiota modulates structural and functional changes in the amygdala, a critical brain area for social and fear-related behaviors associated with neuropsychiatric disorders.
“Indeed, the gut microbiota is reported to modulate structural and functional changes in the amygdala, a critical brain area for social and fear-related behaviors, which are associated with a variety of neuropsychiatric disorders [165].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [165]
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Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
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The central nervous system and the gut microbiome
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Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice
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Stress & the gut-brain axis: Regulation by the microbiome
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Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
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Kynurenine pathway metabolism and the microbiota-gut-brain axis
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Exercise Modifies the Gut Microbiota with Positive Health Effects
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Regulation of prefrontal cortex myelination by the microbiota
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Self-citationEmerging Roles for the Gut Microbiome in Autism Spectrum Disorder
Vuong, H. E., & Hsiao, E. Y. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.024 · Cited by 595 · see citing works
The microbiome and host behavior
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Autism Spectrum Disorders and the Gut Microbiota
Fattorusso, A., Di Genova, L., Dell’Isola, G., Mencaroni, E., & Esposito, S. (2019) · Nutrients · doi:10.3390/nu11030521 · Cited by 484 · see citing works
Gut microbiota and the neuroendocrine system
Farzi, A., Fröhlich, E. E., & Holzer, P. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0600-5 · Cited by 478 · see citing works
Influence of gut microbiota on neuropsychiatric disorders
Cénit, M. C., Sanz, Y., & Codoñer‐Franch, P. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i30.5486 · Cited by 418 · see citing works
Relationship between the gut microbiome and brain function
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The Role of the Microbiome in the Developmental Origins of Health and Disease
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Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
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The Microbiome in Psychology and Cognitive Neuroscience
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Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish
Borrelli, L., Aceto, S., Agnisola, C., De Paolo, S., Dipineto, L., Stilling, R. M., Dinan, T. G., Cryan, J. F., Menna, L. F., & Fioretti, A. (2016) · Scientific Reports · doi:10.1038/srep30046 · Cited by 225 · see citing works
“Previous studies on the gut-brain axis in rodent models have repeatedly shown altered expression of bdnf in certain brain regions under various conditions 7,8,14,15,17 .”
Self-citationMicrobiome profiling reveals gut dysbiosis in a transgenic mouse model of Huntington's disease
Kong, G., Cao, K.-A. L., Judd, L. M., Li, S., Renoir, T., & Hannan, A. J. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.09.001 · Cited by 212 · see citing works
The Role of Gut Bacterial Metabolites in Brain Development, Aging and Disease
Tran, S. M.-S., & Mohajeri, M. H. (2021) · Nutrients · doi:10.3390/nu13030732 · Cited by 207 · see citing works
Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions
Ristori, M. V., Quagliariello, A., Reddel, S., Ianiro, G., Vicari, S., Gasbarrini, A., & Putignani, L. (2019) · Nutrients · doi:10.3390/nu11112812 · Cited by 214 · see citing works
Host microbiota modulates development of social preference in mice
Arentsen, T., Raith, H., Qian, Y., Forssberg, H., & Heijtz, R. D. (2015) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v26.29719 · Cited by 202 · see citing works
Microbial regulation of microRNA expression in the amygdala and prefrontal cortex
Hoban, A. E., Stilling, R. M., M. Moloney, G., Moloney, R. D., Shanahan, F., Dinan, T. G., Cryan, J. F., & Clarke, G. (2017) · Microbiome · doi:10.1186/s40168-017-0321-3 · Cited by 177 · see citing works
Cowan, 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
The microbiome regulates amygdala-dependent fear recall
Hoban, A. E., Stilling, R. M., Moloney, G., Shanahan, F., Dinan, T. G., Clarke, G., & Cryan, J. F. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.100 · Cited by 197 · see citing works
The Role of Gut Dysbiosis in the Pathophysiology of Neuropsychiatric Disorders
Anand, N., Gorantla, V. R., & Chidambaram, S. B. (2022) · Cells · doi:10.3390/cells12010054 · Cited by 185 · see citing works
The contribution of the gut microbiome to neurodevelopment and neuropsychiatric disorders
Warner, B. B. (2018) · Pediatric Research · doi:10.1038/s41390-018-0191-9 · Cited by 168 · see citing works
Microbiota regulates visceral pain in the mouse
Luczynski, P., Tramullas, M., Viola, M. F., Shanahan, F., Clarke, G. A., O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2017) · eLife · doi:10.7554/elife.25887 · Cited by 166 · see citing works
Poor cognitive ageing: Vulnerabilities, mechanisms and the impact of nutritional interventions
Miquel, S., Champ, C., Day, J. E. L., Aarts, E., Bahr, B. A., Bakker, M. J., Bánáti, D., Calabrese, V., Cederholm, T., Cryan, J. F., et al. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.12.004 · Cited by 163 · see citing works
Kadosh, K. C., Muhardi, L., Parikh, P., Basso, M., Mohamed, H. J. J., Prawitasari, T., Samuel, F. O., Ma, G., & Geurts, J. M. W. (2021) · Nutrients · doi:10.3390/nu13010199 · Cited by 186 · see citing works
The Impact of Gut Microbiota Disorders on the Blood–Brain Barrier
Wei, T., Zhu, H., Feng, Y., Guo, R., & Wan, D. (2020) · Infection and Drug Resistance · doi:10.2147/idr.s254403 · Cited by 163 · see citing works
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MicroRNAs as biomarkers for major depression: a role for let-7b and let-7c
Gururajan, A., Naughton, M., Scott, K. A., O’Connor, R. M., Moloney, G. M., Clarke, G. A., Dowling, J. L., Walsh, A. E. L., Ismail, M. F., Shorten, G., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.131 · Cited by 144 · see citing works
The role of the microbiome in the neurobiology of social behaviour
Sarkar, A., Harty, S., Johnson, K. V. ‐., Moeller, A. H., Carmody, R. N., Lehto, S. M., Erdman, S. E., Dunbar, R. I. M., & Burnet, P. W. J. (2020) · Biological Reviews · doi:10.1111/brv.12603 · Cited by 135 · see citing works
Gao, W., Salzwedel, A., Carlson, A. L., Xia, K., Azcárate-Peril, M. A., Styner, M. A., Thompson, A. L., Geng, X., Goldman, B. D., Gilmore, J. H., et al. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5161-8 · Cited by 127 · see citing works
Altered Gut Microbiota Related to Inflammatory Responses in Patients With Huntington’s Disease
Du, G., Dong, W., Yang, Q., Yu, X., Ma, J., Gu, W., & Huang, Y. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.603594 · Cited by 124 · see citing works
Mutual Interactions among Exercise, Sport Supplements and Microbiota
Zeppa, S. D., Agostini, D., Gervasi, M., Annibalini, G., Amatori, S., Ferrini, F., Sisti, D., Piccoli, G., Barbieri, E., Sestili, P., et al. (2019) · Nutrients · doi:10.3390/nu12010017 · Cited by 122 · see citing works
Gut Microbiota, Inflammation, and Probiotics on Neural Development in Autism Spectrum Disorder
Doenyas, C. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.01.060 · Cited by 121 · see citing works
The role of the gut microbiome in the development of schizophrenia
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G. A., & Dinan, T. G. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2020.02.010 · Cited by 119 · 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
The roles of the gut microbiota–miRNA interaction in the host pathophysiology
Li, M., Chen, W., & Wang, Y. (2020) · Molecular Medicine · doi:10.1186/s10020-020-00234-7 · Cited by 110 · see citing works
Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice
Stilling, R. M., Moloney, G. M., Ryan, F. J., Hoban, A. E., Bastiaanssen, T. F., Shanahan, F., Clarke, G., Claesson, M. J., Dinan, T. G., & Cryan, J. F. (2018) · eLife · doi:10.7554/elife.33070 · Cited by 106 · see citing works
Self-citationGut Microbiota Interaction with the Central Nervous System throughout Life
Ojeda, J., Ávila, A., & Vidal, P. M. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10061299 · Cited by 107 · see citing works
Liu, F., Horton-Sparks, K., Hull, V. L., Li, R. W., & Martínez‐Cerdeño, V. (2018) · Molecular Autism · doi:10.1186/s13229-018-0251-3 · Cited by 104 · see citing works
Mitochondrial function and abnormalities implicated in the pathogenesis of ASD
Castora, F. J. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.12.015 · Cited by 104 · see citing works
Maternal prenatal gut microbiota composition predicts child behaviour
Dawson, S. L., O’Hely, M., Jacka, F. N., Ponsonby, A., Symeonides, C., Loughman, A., Collier, F., Moreno‐Betancur, M., Sly, P. D., Burgner, D. P., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103400 · Cited by 100 · see citing works
Gut microbiota and central nervous system development
Principi, N., & Esposito, S. (2016) · Journal of Infection · doi:10.1016/j.jinf.2016.09.010 · Cited by 92 · see citing works
Intervention strategies for cesarean section–induced alterations in the microbiota-gut-brain axis
Moya-Pérez, Á., Luczynski, P., Renes, I. B., Wang, S., Borre, Y. E., Ryan, C. A., Knol, J., Stanton, C., Dinan, T. G., & Cryan, J. F. (2017) · Nutrition Reviews · doi:10.1093/nutrit/nuw069 · Cited by 95 · see citing works
The connection between microbiome and schizophrenia
Golofast, B., & Vales, K. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.011 · 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
Gut Microbiome Signatures Are Biomarkers for Cognitive Impairment in Patients With Ischemic Stroke
Ling, Y., Gong, T., Zhang, J., Gu, Q., Gao, X., Weng, X., Liu, J., & Sun, J. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.511562 · Cited by 92 · see citing works
Gut microbiota, kynurenine pathway and mental disorders – Review
Więdłocha, M., Marcinowicz, P., Janoska-Jaździk, M., & Szulc, A. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110145 · Cited by 87 · see citing works
The Brain-Gut-Microbiome System: Pathways and Implications for Autism Spectrum Disorder
Chernikova, M. A., Flores, G. D., Kilroy, E., Labus, J. S., Mayer, E. A., & Aziz‐Zadeh, L. (2021) · Nutrients · doi:10.3390/nu13124497 · Cited by 86 · see citing works
The gut microbiome of laboratory mice: considerations and best practices for translational research
Ericsson, A. C., & Franklin, C. L. (2021) · Mammalian Genome · doi:10.1007/s00335-021-09863-7 · Cited by 85 · see citing works
Visceral Inflammation and Immune Activation Stress the Brain
Holzer, P., Farzi, A., Hassan, A. M., Zenz, G., Jačan, A., & Reichmann, F. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01613 · Cited by 84 · see citing works
Gut Microbiome Composition is Associated with Age and Memory Performance in Pet Dogs
Enikö Kubinyi, B., Rhali, S. B., Sándor, S., Szabó, A., & Felföldi, T. (2020) · Animals · doi:10.3390/ani10091488 · Cited by 82 · see citing works
Gut-brain axis: A matter of concern in neuropsychiatric disorders…!
Naveed, M., Zhou, Q.-G., Chu, X., Taleb, A., Meng, F. J., Ahmed, B., Zhang, Y., Fukunaga, K., & Han, F. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110051 · Cited by 81 · see citing works
A biological framework for emotional dysregulation in alcohol misuse: from gut to brain
Carbia, C., Lannoy, S., Maurage, P., López‐Caneda, E., O’Riordan, K. J., Dinan, T. G., & Cryan, J. F. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00970-6 · Cited by 80 · see citing works
Johnstone, N., Milesi, C., Burn, O., van den Bogert, B., Nauta, A., Hart, K. H., Sowden, P. T., Burnet, P. W. J., & Kadosh, K. C. (2021) · Scientific Reports · doi:10.1038/s41598-021-87865-w · Cited by 84 · see citing works
Microbiome Gut-Brain-Axis: Impact on Brain Development and Mental Health
Ramadan, Y. N., Alqifari, S. F., Alshehri, K., Alhowiti, A., Mirghani, H. O., Alrasheed, T., Aljohani, F., Alghamdi, A. M., & Hetta, . F. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04846-0 · Cited by 90 · see citing works
The microbiota, the gut and the brain in eating and alcohol use disorders: A ‘Ménage à Trois’?
Temko, J. E., Bouhlal, S., Farokhnia, M., Lee, M. R., Cryan, J. F., & Leggio, L. (2017) · Alcohol and Alcoholism · doi:10.1093/alcalc/agx024 · Cited by 76 · see citing works
Microbiome in brain function and mental health
Kennedy, P. J., Murphy, A., Cryan, J. F., Ross, R. P., Dinan, T. G., & Stanton, C. (2016) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2016.05.001 · Cited by 76 · see citing works
The Brain-Gut-Microbiome Axis: What Role Does it Play in Autism Spectrum Disorder?
Luna, R. A., Savidge, T., & Williams, K. C. (2016) · Current Developmental Disorders Reports · doi:10.1007/s40474-016-0077-7 · Cited by 73 · see citing works
Microbiota and Neurodevelopmental Trajectories: Role of Maternal and Early-Life Nutrition
Codagnone, M. G., Stanton, C., O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2019) · Annals of Nutrition and Metabolism · doi:10.1159/000499144 · Cited by 73 · see citing works
Old Friends, immunoregulation, and stress resilience
Langgartner, D., Lowry, C. A., & Reber, S. O. (2018) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-018-2228-7 · Cited by 73 · see citing works
Kigerl, K. A., Zane, K., Adams, K., Sullivan, M. B., & Popovich, P. G. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113085 · Cited by 70 · see citing works
Perioperative neurocognitive dysfunction: thinking from the gut?
Xu, X., Hu, Y., Yan, E., Zhan, G., Liu, C., & Yang, C. (2020) · Aging · doi:10.18632/aging.103738 · Cited by 69 · see citing works
Moloney, G. M., O’Leary, O. F., Salvo-Romero, E., Desbonnet, L., Shanahan, F., Dinan, T. G., Clarke, G., & Cryan, J. F. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.07.026 · Cited by 68 · see citing works
Salami, M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.613120 · Cited by 67 · see citing works
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- Authors
- Stilling, R. M., Ryan, F. J., Hoban, A. E., Shanahan, F., Clarke, G., Claesson, M. J., Dinan, T. G., & Cryan, J. F.
- Affiliations
- University College Cork (IE)
- Corresponding author
- Stilling, Roman M.
- Cryan, John F.
- ORCID
- Venue
- Brain Behavior and Immunity
- Publisher
- Elsevier BV
- Published
- 2015-11
- Volume
- 50
- Pages
- 209-220
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W889536224
- Cited by
- 233
- References
- 106
- Citations by year
- 2026: 12 · 2025: 11 · 2024: 20 · 2023: 15 · 2022: 17 · 2021: 27 · 2020: 30 · 2019: 27 · 2018: 26 · 2017: 19 · 2016: 26 · 2015: 3
- FWCI
- 10.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Science Foundation Ireland (07/CE/B1368, 12/RC/2273, 11/SIRG/B2162)
- Irish Research Council (GOIPD/2014/355)
- Dept. of Agriculture, Food & Fisheries and Forestry and Enterprise Ireland
- Brain and Behavior Research Foundation (20771)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- gut microbiota, germ-free mice, amygdala, brain development, host-microbe interactions, anxiety-like behavior, social behavior, immediate early genes, gene expression, exon usage, RNA editing, neuronal activity, neurodevelopmental disorders
- MeSH terms
- Amygdala, Animals, Interpersonal Relations, Male, Neurons, Signal Transduction, Genes, Immediate-Early, Gene Expression Profiling, Mice, Microbiota
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