The DOI matches its Crossref record; 105 of the 106 references it cites were found in a registry or an index.
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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In the citing paper
“GF mice display heightened expression of transcription factors related to neuronal activation (e.g., fos) in the amygdala relative to conventional controls (Stilling et al., 2015).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Stilling et al., 2015
In the citing paper
“GF animals have altered expression of genes implicated in neurophysiology in the amygdala (Stilling et al., 2015) and hippocampus (Chen et al., 2017a) (see Table 2).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Stilling et al., 2015
In the citing paper
“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
In the citing paper
“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]
Citations
Cites
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106
Trimmomatic: a flexible trimmer for Illumina sequence data
Bolger, A. M., Lohse, M., & Usadel, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu170 · Cited by 65,548
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464
Differential expression analysis for sequence count data
Anders, S., & Huber, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-10-r106 · Cited by 15,581
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn923 · Cited by 14,108
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
Edgar, R. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.207 · Cited by 13,288
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572
Structural and functional features of central nervous system lymphatic vessels
Louveau, A., Smirnov, I., Keyes, T. J., Eccles, J. D., Rouhani, S. J., Peske, J. D., Derecki, N. C., Castle, D., Mandell, J. W., Lee, K. S., et al. (2015) · Nature · doi:10.1038/nature14432 · Cited by 4,413
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888
Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice
Ridaura, V. K., Faith, J. J., Rey, F. E., Cheng, J., Duncan, A. E., Kau, A. L., Griffin, N. W., Lombard, V., Henrissat, B., Bain, J. R., et al. (2013) · Science · doi:10.1126/science.1241214 · Cited by 3,788
Host microbiota constantly control maturation and function of microglia in the CNS
Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4030 · Cited by 3,569
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · cited 1×
“…centre for evaluating and responding to social stimuli, in addition to being critically involved in anxiety and fear-related behaviours and memory (Allsop et al., 2014; Amaral, 2003; Kliemann et al., 2012; Noonan et al., 2014; Phelps and LeDoux, 2005; Sabatini et al., 2007; Sallet et al., 2011).”
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735
Mechanisms underlying the resistance to diet-induced obesity in germ-free mice
Bäckhed, F., Manchester, J. K., Semenkovich, C. F., & Gordon, J. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605374104 · Cited by 2,615
Gut–brain axis: How the microbiome influences anxiety and depression
Foster, J. A., & McVey Neufeld, K.-A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.005 · Cited by 2,460
Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.77 · Cited by 1,893
Self-citationBercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748
Sample criteria for testing outlying observations
Grubbs, F. E. (1950) · The Annals of Mathematical Statistics · doi:10.1214/aoms/1177729885 · Cited by 1,631
The interplay between the intestinal microbiota and the brain
Collins, S. M., Surette, M., & Bercik, P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2876 · Cited by 1,611 · cited 1×
“It is now increasingly acknowledged that host-associated microbes are intimately involved in host development, brain function and behaviour (Collins et al., 2012; Cryan and Dinan, 2012; Lyte, 2013; Mayer et al., 2014a).”
Ca2+ Influx Regulates BDNF Transcription by a CREB Family Transcription Factor-Dependent Mechanism
Tao, X., Finkbeiner, S., Arnold, D. B., Shaywitz, A. J., & Greenberg, M. E. (1998) · Neuron · doi:10.1016/s0896-6273(00)81010-7 · Cited by 1,561
Detecting differential usage of exons from RNA-seq data
Anders, S., Reyes, A., & Huber, W. (2012) · Genome Research · doi:10.1101/gr.133744.111 · Cited by 1,545
Gaze fixation and the neural circuitry of face processing in autism
Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., Alexander, A. L., & Davidson, R. J. (2005) · Nature Neuroscience · doi:10.1038/nn1421 · Cited by 1,543
Gut/brain axis and the microbiota
Mayer, E. A., Tillisch, K., & Gupta, A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76304 · Cited by 1,503
Clemson, C. M., Hutchinson, J. N., Sara, S. A., Ensminger, A. W., Fox, A. H., Chess, A., & Lawrence, J. B. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.01.026 · Cited by 1,445
Epigenetic regulation in psychiatric disorders
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2132 · Cited by 1,400
GSEA-P : a desktop application for Gene Set Enrichment Analysis
Subramanian, A., Kuehn, H., Gould, J., Tamayo, P., & Mesirov, J. P. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm369 · Cited by 1,399
Neufeld, K. M., Kang, N., Bienenstock, J., & Foster, J. A. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01620.x · Cited by 1,392
Consumption of fermented milk product with probiotic modulates brain activity
Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain–Raspaud, S., Trotin, B., Naliboff, B., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.02.043 · Cited by 1,192
Microbiota and neurodevelopmental windows: implications for brain disorders
Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.05.002 · Cited by 1,089
Gut microbes and the brain: paradigm shift in neuroscience
Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F., & Tillisch, K. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3299-14.2014 · Cited by 1,033
Mathelier, A., Zhao, X., Zhang, A. W., Parcy, F., Worsley-Hunt, R., Arenillas, D. J., Buchman, S., Chen, C., Chou, A., Ienasescu, H., et al. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt997 · Cited by 983
Altered Histone Acetylation Is Associated with Age-Dependent Memory Impairment in Mice
Peleg, S., Sananbenesi, F., Zovoilis, A., Burkhardt, S., Bahari-Javan, S., Agis-Balboa, R. C., Cota, P., Wittnam, J. L., Gogol-Doering, A., Opitz, L., et al. (2010) · Science · doi:10.1126/science.1186088 · Cited by 951
Microbiota is essential for social development in the mouse
Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.65 · Cited by 866
Influences of microbiota on intestinal immune system development.
Cebra, J. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/69.5.1046s · Cited by 819
Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour
Desbonnet, L., Clarke, G., Traplin, A., O’Sullivan, O., Crispie, F., Moloney, R. D., Cotter, P. D., Dinan, T. G., & Cryan, J. F. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.04.004 · Cited by 760
Identification of a Signaling Pathway Involved in Calcium Regulation of BDNF Expression
Shieh, P. B., Hu, S.-C., Bobb, K., Timmusk, T., & Ghosh, A. (1998) · Neuron · doi:10.1016/s0896-6273(00)81011-9 · Cited by 693
Bercik, P., Verdu, E. F., Foster, J. A., Macri, J., Potter, M., Huang, X., Malinowski, P., Jackson, W., Blennerhassett, P., Neufeld, K. A., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.06.063 · Cited by 674
Microbial genes, brain & behaviour – epigenetic regulation of the gut–brain axis
Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12109 · Cited by 637
Crumeyrolle-Arias, M., Jaglin, M., Bruneau, A., Vancassel, S., Cardona, A., Daugé, V., Naudon, L., & Rabot, S. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.01.014 · Cited by 581
Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology
Dinan, T. G., & Cryan, J. F. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.007 · Cited by 577
Self-citationVagal pathways for microbiome-brain-gut axis communication
Forsythe, P., Bienenstock, J., & Kunze, W. A. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_5 · Cited by 576
Collective unconscious: How gut microbes shape human behavior
Dinan, T. G., Stilling, R. M., Stanton, C., & Cryan, J. F. (2015) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2015.02.021 · Cited by 571
RADAR: a rigorously annotated database of A-to-I RNA editing
Ramaswami, G., & Li, J. B. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt996 · Cited by 534
Social networks predict gut microbiome composition in wild baboons
Tung, J., Barreiro, L. B., Burns, M. B., Grenier, J., Lynch, J., Grieneisen, L., Jeanne Altmann, A., Alberts, S. C., Blekhman, R., & Archie, E. A. (2015) · eLife · doi:10.7554/elife.05224 · Cited by 530
Social Network Size Affects Neural Circuits in Macaques
Sallet, J., Mars, R. B., Noonan, M. P., Andersson, J. L., O’Reilly, J. X., Jbabdi, S., Croxson, P. L., Jenkinson, M., Miller, K. L., & Rushworth, M. F. S. (2011) · Science · doi:10.1126/science.1210027 · Cited by 514
Adult hippocampal neurogenesis is regulated by the microbiome
Ogbonnaya, E. S., Clarke, G., Shanahan, F., Dinan, T. G., Cryan, J. F., & O’Leary, O. F. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.023 · Cited by 491
Brühl, A. B., Delsignore, A., Komossa, K., & Weidt, S. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.003 · Cited by 439
Lyte, M. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003726 · Cited by 399
Isolation and characterization of a dual-substrate phosphodiesterase gene family: PDE10A
Soderling, S. H., Bayuga, S. J., & Beavo, J. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.12.7071 · Cited by 374
REDItools: high-throughput RNA editing detection made easy
Picardi, E., & Pesole, G. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt287 · Cited by 359
Epigenetic sources of behavioral differences in mice
Francis, D. D., Szegda, K. L., Campbell, G., Martin, W. D., & Insel, T. R. (2003) · Nature Neuroscience · doi:10.1038/nn1038 · Cited by 334
Effects of intestinal microbiota on anxiety-like behavior
Neufeld, K.-A. M., Kang, N., Bienenstock, J., & Foster, J. A. (2011) · Communicative & Integrative Biology · doi:10.4161/cib.15702 · Cited by 311
Altered brain-gut axis in autism: comorbidity or causative mechanisms
Mayer, E. A., Padua, D., & Tillisch, K. (2014) · BioEssays · doi:10.1002/bies.201400075 · Cited by 304
Amygdala Volume and Nonverbal Social Impairment in Adolescent and Adult Males With Autism
Nacewicz, B. M., Dalton, K. M., Johnstone, T., Long, M. T., McAuliff, E. M., Oakes, T. R., Alexander, A. L., & Davidson, R. J. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.12.1417 · Cited by 302
McVey Neufeld, K. A., Mao, Y. K., Bienenstock, J., Foster, J. A., & Kunze, W. A. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12049 · Cited by 299
The amygdala, social behavior, and danger detection
AMARAL, D. G. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1280.015 · Cited by 293
Goehler, L. E., Park, S. M., Opitz, N., Lyte, M., & Gaykema, R. P. A. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.08.009 · Cited by 287
Frey, S., Bergado, J. A., Seidenbecher, T., Pape, H., & Frey, J. U. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-10-03697.2001 · Cited by 260
Reduced Neural Habituation in the Amygdala and Social Impairments in Autism Spectrum Disorders
Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., & Aylward, E. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2008.07101681 · Cited by 255
Kawashima, T., Okuno, H., Nonaka, M., Adachi-Morishima, A., Yagishita-Kyo, N., Okamura, M., Takemoto‐Kimura, S., Worley, P. F., & Bito, H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806518106 · Cited by 252
Microbial Endocrinology: The Microbiota-Gut-Brain Axis in Health and Disease
Lyte, M., & Cryan, J. F. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0897-4 · Cited by 240
O’Tuathaigh, C. M. P., Babovic, D., O’Sullivan, G. J., Clifford, J. J., Tighe, O., Croke, D. T., Harvey, R. P., & Waddington, J. L. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.03.051 · Cited by 238
Control of human potassium channel inactivation by editing of a small mRNA hairpin
Bhalla, T., Rosenthal, J. J. C., Holmgren, M., & Reenan, R. A. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb825 · Cited by 227
Collins, S. M., Kassam, Z., & Berčík, P. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.06.004 · Cited by 214
Pecqueur, C., Bui, T., Gelly, C., Hauchard, J., Barbot, C., Bouillaud, F., Ricquier, D., Miroux, B., & Thompson, C. B. (2008) · The FASEB Journal · doi:10.1096/fj.07-8945com · Cited by 209
Evolutionarily conserved human targets of adenosine to inosine RNA editing
Levanon, E. Y. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki239 · Cited by 206
Arseneault-Bréard, J., Rondeau, I., Gilbert, K., Girard, S.-A., Tompkins, T. A., Godbout, R., & Rousseau, G. (2012) · British Journal of Nutrition · doi:10.1017/s0007114511005137 · Cited by 205
Oxytocin receptor gene methylation: converging multilevel evidence for a role in social anxiety
Ziegler, C., Dannlowski, U., Bräuer, D., Stevens, S., Laeger, I., Wittmann, H., Kugel, H., Dobel, C., Hurlemann, R., Reif, A., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.2 · Cited by 193
A neural circuit covarying with social hierarchy in macaques
Noonan, M. P., Sallet, J., Mars, R. B., Neubert, F. X., O'Reilly, J. X., Andersson, J. L., Mitchell, A. S., Bell, A. H., Miller, K. L., & Rushworth, M. F. S. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001940 · Cited by 183
The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders
Kliemann, D., Dziobek, I., Hatri, A., Baudewig, J., & Heekeren, H. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5294-11.2012 · Cited by 183
Evolutionarily conserved human targets of adenosine to inosine RNA editing
Levanon, E. Y., Hallegger, M., Kinar, Y., Shemesh, R., Djinović‐Carugo, K., Rechavi, G., Jantsch, M. F., & Eisenberg, E. (2005) · Cited by 181
Adult mouse brain gene expression patterns bear an embryologic imprint
Zapala, M. A., Hovatta, I., Ellison, J. A., Wodicka, L. M., Rio, J. A. D., Tennant, R. S., Tynan, W., Broide, R. S., Helton, R., Stoveken, B. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503357102 · Cited by 177
Genomics of schizophrenia: time to consider the gut microbiome?
Dinan, T. G., Borre, Y. E., & Cryan, J. F. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.93 · Cited by 177
Gut Vagal Afferents Differentially Modulate Innate Anxiety and Learned Fear
Klarer, M., Arnold, M., Günther, L., Winter, C., Langhans, W., & Meyer, U. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0252-14.2014 · Cited by 159
High levels of RNA-editing site conservation amongst 15 laboratory mouse strains
Danecek, P., Nellåker, C., McIntyre, R. E., Buendia-Buendia, J. E., Bumpstead, S., Ponting, C. P., Flint, J., Durbin, R. M., Keane, T., & Adams, D. J. (2012) · Genome biology · doi:10.1186/gb-2012-13-4-r26 · Cited by 159
The Neuronal Activity-Driven Transcriptome
Benito, E., & Barco, Á. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8772-z · Cited by 152
Optogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150
Stilling, R. M., Bordenstein, S. R., Dinan, T. G., & Cryan, J. F. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00147 · Cited by 139
Goehler, L. E., Lyte, M., & Gaykema, R. P. A. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.02.005 · Cited by 127
Amygdala Gene Expression Correlates of Social Behavior in Monkeys Experiencing Maternal Separation
Sabatini, M. J., Ebert, P., Lewis, D. A., Levitt, P., Cameron, J. L., & Mirnics, K. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4765-06.2007 · Cited by 125
cAMP Response Element-Binding Protein Is a Primary Hub of Activity-Driven Neuronal Gene Expression
Benito, E., Valor, L. M., Jimenez-Minchan, M., Huber, W. K., & Barco, Á. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4554-11.2011 · Cited by 119
Stilling, R. M., Benito, E., Barth, J., Gertig, M., Capece, V., Burckhardt, S., Bonn, S., & Fischer, A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00373 · Cited by 115
Identification and characterization of a virus-inducible non-coding RNA in mouse brain
Saha, S., Murthy, S., & Rangarajan, P. N. (2006) · Journal of General Virology · doi:10.1099/vir.0.81768-0 · Cited by 111
Darned in 2013: inclusion of model organisms and linking with Wikipedia
Kiran, A. M., O'Mahony, J. J., Sanjeev, K., & Baranov, P. V. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks961 · Cited by 110
Obadiah, J. M., Avidor‐Reiss, T., Fishburn, C. S., Carmon, S., Bayewitch, M. L., Vogel, Z., Fuchs, S., & Levavi‐Sivan, B. (1999) · Cellular and Molecular Neurobiology · doi:10.1023/a:1006988603199 · Cited by 94
Kirby, E. D., Friedman, A. R., Covarrubias, D., Ying, C., Sun, W. G., Goosens, K. A., Sapolsky, R. M., & Kaufer, D. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.71 · Cited by 88
The Amygdala, Autism and Anxiety
Amaral, D. G., & Corbett, B. A. (2003) · Novartis Foundation symposium · doi:10.1002/0470869380.ch11 · Cited by 73
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Kim, G., Arseneault-Bréard, J., Monaco, F. F., Beaudoin, A., Bah, T. M., Tompkins, T. A., Godbout, R., & Rousseau, G. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114512003807 · Cited by 68
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Stulić, M., & Jantsch, M. F. (2013) · RNA Biology · doi:10.4161/rna.26216 · Cited by 50
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Gonzalez, C. L., López-Rodríguez, A., Srikumar, D., Rosenthal, J. J. C., & Holmgren, M. (2011) · Nature Communications · doi:10.1038/ncomms1446 · Cited by 32
Rodríguez-Tornos, F. M., Orbegozo, I. S. A., Cubelos, B., & Nieto, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053848 · Cited by 31
Vuoristo, J. T., Berrettini, W. H., Overhauser, J., Prockop, D. J., Ferraro, T. N., & Ala‐Kokko, L. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000758 · Cited by 29
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Lagarrigue, S., Hormozdiari, F., Martin, L. J., Lecerf, F., Hasin-Brumshtein, Y., Rau, C., Hagopian, R., Xiao, Y., Yan, J., Drake, T. A., et al. (2013) · Genetics · doi:10.1534/genetics.112.149054 · Cited by 25
Baev, K. V. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00053-6 · Cited by 22
García-Medina, N. E., & Miranda, M. I. (2012) · Brain stimulation · doi:10.1016/j.brs.2012.03.020 · Cited by 19
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McDougall, S. J., & Andresen, M. C. (2008) · The FASEB Journal · doi:10.1096/fasebj.22.1_supplement.1171.9 · Cited by 1
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Metadata
- 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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