Mechanisms Underlying Microbial-Mediated Changes in Social Behavior in Mouse Models of Autism Spectrum Disorder

Neuron

Volumn 101, Issue 2, 2019, Pages 246-259.e6

  Sgritta, Martina ^a   Dooling, Sean W ^a   Buffington, Shelly A ^a   Momin, Eric N ^a   Francis, Michael B ^a   Britton, Robert A ^a   Costa Mattioli, Mauro ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

autism; dopamine; gut microbiota brain axis; microbiome; oxytocin; probiotic; social behavior; vagus nerve

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; CIRCULATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTROPHYSIOLOGY; GENETIC VARIABILITY; IMMUNOHISTOCHEMISTRY; LACTOBACILLUS REUTERI; MEMBRANE PERMEABILITY; MICROBIAL COMMUNITY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHYLOGENY; PRINCIPAL COORDINATE ANALYSIS; PRIORITY JOURNAL; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM; ACTION POTENTIAL; ANIMAL; ANTISOCIAL PERSONALITY DISORDER; CAPILLARY PERMEABILITY; COMPLICATION; DISEASE MODEL; DRUG EFFECT; EXPLORATORY BEHAVIOR; GENETICS; HUMAN; HUMAN RELATION; INTESTINE FLORA; MALE; METABOLISM; ODOR; PHYSIOLOGY; TRANSGENIC MOUSE;

BENZOXAZINE DERIVATIVE; CENTRAL STIMULANT AGENT; DOPAMINE TRANSPORTER; L 371257; NERVE PROTEIN; OXTR PROTEIN, MOUSE; OXYTOCIN RECEPTOR; PICROTOXIN; PIPERIDINE DERIVATIVE; SHANK3 PROTEIN, MOUSE; VALPROIC ACID;

ACTION POTENTIALS; ANIMALS; AUTISM SPECTRUM DISORDER; BENZOXAZINES; CAPILLARY PERMEABILITY; CENTRAL NERVOUS SYSTEM STIMULANTS; DISEASE MODELS, ANIMAL; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; EXPLORATORY BEHAVIOR; GASTROINTESTINAL MICROBIOME; HUMANS; INTERPERSONAL RELATIONS; LACTOBACILLUS REUTERI; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PICROTOXIN; PIPERIDINES; RECEPTORS, OXYTOCIN; SMELL; SOCIAL BEHAVIOR DISORDERS; VALPROIC ACID;

EID: 85059826502     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2018.11.018     Document Type: Article

References (101)

1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (DSM-5). 2013, American Psychiatric Pub.
2. Arentsen, T., Raith, H., Qian, Y., Forssberg, H., Diaz Heijtz, R., Host microbiota modulates development of social preference in mice. Microb. Ecol. Health Dis., 26, 2015, 29719.
3. Baio, J., Wiggins, L., Christensen, D.L., Maenner, M.J., Daniels, J., Warren, Z., Kurzius-Spencer, M., Zahorodny, W., Robinson Rosenberg, C., White, T., et al. (2018). Prevalence of autism spectrum disorder among children aged 8 years—autism and developmental disabilities monitoring network, 11 Sites, United States, 2014. Morbidity and Mortality Weekly Report Surveillance Summaries (Washington, DC: 2002) 67, 1–23.
4. Bariselli, S., Tzanoulinou, S., Glangetas, C., Prévost-Solié C., Pucci, L., Viguié J., Bezzi, P., O'Connor, E.C., Georges, F., Lüscher, C., Bellone, C., SHANK3 controls maturation of social reward circuits in the VTA. Nat. Neurosci. 19 (2016), 926–934.
5. Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N., Golani, I., Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 125 (2001), 279–284.
6. Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K.D., et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141 (2011), 599–609.
7. Bercik, P., Park, A.J., Sinclair, D., Khoshdel, A., Lu, J., Huang, X., Deng, Y., Blennerhassett, P.A., Fahnestock, M., Moine, D., et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol. Motil. 23 (2011), 1132–1139.
8. Bertola, A., Mathews, S., Ki, S.H., Wang, H., Gao, B., Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat. Protoc. 8 (2013), 627–637.
9. Borre, Y.E., O'Keeffe, G.W., Clarke, G., Stanton, C., Dinan, T.G., Cryan, J.F., Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol. Med. 20 (2014), 509–518.
10. Bravo, J.A., Forsythe, P., Chew, M.V., Escaravage, E., Savignac, H.M., Dinan, T.G., Bienenstock, J., Cryan, J.F., Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. USA 108 (2011), 16050–16055.
11. Buffington, S.A., Di Prisco, G.V., Auchtung, T.A., Ajami, N.J., Petrosino, J.F., Costa-Mattioli, M., Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165 (2016), 1762–1775.
12. Christensen, J., Grønborg, T.K., Sørensen, M.J., Schendel, D., Parner, E.T., Pedersen, L.H., Vestergaard, M., Prenatal valproate exposure and risk of autism spectrum disorders and childhood autism. JAMA 309 (2013), 1696–1703.
13. Coretti, L., Cristiano, C., Florio, E., Scala, G., Lama, A., Keller, S., Cuomo, M., Russo, R., Pero, R., Paciello, O., et al. Sex-related alterations of gut microbiota composition in the BTBR mouse model of autism spectrum disorder. Sci. Rep., 7, 2017, 45356.
14. De Angelis, M., Piccolo, M., Vannini, L., Siragusa, S., De Giacomo, A., Serrazzanetti, D.I., Cristofori, F., Guerzoni, M.E., Gobbetti, M., Francavilla, R., Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS ONE, 8, 2013, e76993.
15. Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T.G., Cryan, J.F., Microbiota is essential for social development in the mouse. Mol. Psychiatry 19 (2014), 146–148.
16. Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M.L., Forssberg, H., Pettersson, S., Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. USA 108 (2011), 3047–3052.
17. Ding, H.T., Taur, Y., Walkup, J.T., Gut microbiota and autism: key concepts and findings. J. Autism Dev. Disord. 47 (2017), 480–489.
18. Dölen, G., Darvishzadeh, A., Huang, K.W., Malenka, R.C., Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501 (2013), 179–184.
19. Donaldson, Z.R., Young, L.J., Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322 (2008), 900–904.
20. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
21. Edgar, R.C., UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10 (2013), 996–998.
22. −/− mice. PLoS ONE, 7, 2012, e46837.
23. Falcinelli, S., Rodiles, A., Unniappan, S., Picchietti, S., Gioacchini, G., Merrifield, D.L., Carnevali, O., Probiotic treatment reduces appetite and glucose level in the zebrafish model. Sci. Rep., 6, 2016, 18061.
24. Golubeva, A.V., Joyce, S.A., Moloney, G., Burokas, A., Sherwin, E., Arboleya, S., Flynn, I., Khochanskiy, D., Moya-Pérez, A., Peterson, V., et al. Microbiota-related changes in bile acid and tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism. EBioMedicine 24 (2017), 166–178.
25. Gregory, R., Cheng, H., Rupp, H.A., Sengelaub, D.R., Heiman, J.R., Oxytocin increases VTA activation to infant and sexual stimuli in nulliparous and postpartum women. Horm. Behav. 69 (2015), 82–88.
26. Groppe, S.E., Gossen, A., Rademacher, L., Hahn, A., Westphal, L., Gründer, G., Spreckelmeyer, K.N., Oxytocin influences processing of socially relevant cues in the ventral tegmental area of the human brain. Biol. Psychiatry 74 (2013), 172–179.
27. Gunaydin, L.A., Grosenick, L., Finkelstein, J.C., Kauvar, I.V., Fenno, L.E., Adhikari, A., Lammel, S., Mirzabekov, J.J., Airan, R.D., Zalocusky, K.A., et al. Natural neural projection dynamics underlying social behavior. Cell 157 (2014), 1535–1551.
28. Gupta, J., Nebreda, A.R., Analysis of intestinal permeability in mice. Biol. Protoc., 4, 2014, e1289.
29. Hallmayer, J., Cleveland, S., Torres, A., Phillips, J., Cohen, B., Torigoe, T., Miller, J., Fedele, A., Collins, J., Smith, K., et al. Genetic heritability and shared environmental factors among twin pairs with autism. Arch. Gen. Psychiatry 68 (2011), 1095–1102.
30. Han, W., Tellez, L.A., Perkins, M.H., Perez, I.O., Qu, T., Ferreira, J., Ferreira, T.L., Quinn, D., Liu, Z.W., Gao, X.B., et al. A neural circuit for gut-induced reward. Cell 175 (2018), 887–888.
31. Hara, Y., Ago, Y., Higuchi, M., Hasebe, S., Nakazawa, T., Hashimoto, H., Matsuda, T., Takuma, K., Oxytocin attenuates deficits in social interaction but not recognition memory in a prenatal valproic acid-induced mouse model of autism. Horm. Behav. 96 (2017), 130–136.
32. Harony-Nicolas, H., Kay, M., Hoffmann, J.D., Klein, M.E., Bozdagi-Gunal, O., Riad, M., Daskalakis, N.P., Sonar, S., Castillo, P.E., Hof, P.R., et al. Oxytocin improves behavioral and electrophysiological deficits in a novel Shank3-deficient rat. eLife, 6, 2017, e18904.
33. Holingue, C., Newill, C., Lee, L.C., Pasricha, P.J., Daniele Fallin, M., Gastrointestinal symptoms in autism spectrum disorder: a review of the literature on ascertainment and prevalence. Autism Res. 11 (2018), 24–36.
34. Holmes, J.L., Van Itallie, C.M., Rasmussen, J.E., Anderson, J.M., Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expr. Patterns 6 (2006), 581–588.
35. 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. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155 (2013), 1451–1463.
36. Huang, Y.C., Hessler, N.A., Social modulation during songbird courtship potentiates midbrain dopaminergic neurons. PLoS ONE, 3, 2008, e3281.
37. Huang, W., Placzek, A.N., Di Prisco, G.V., Khatiwada, S., Sidrauski, C., Krnjević K., Walter, P., Dani, J.A., Costa-Mattioli, M., Translational control by eIF2α phosphorylation regulates vulnerability to the synaptic and behavioral effects of cocaine. eLife, 5, 2016, e12052.
38. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
39. Hung, L.W., Neuner, S., Polepalli, J.S., Beier, K.T., Wright, M., Walsh, J.J., Lewis, E.M., Luo, L., Deisseroth, K., Dölen, G., Malenka, R.C., Gating of social reward by oxytocin in the ventral tegmental area. Science 357 (2017), 1406–1411.
40. Indrio, F., Di Mauro, A., Riezzo, G., Civardi, E., Intini, C., Corvaglia, L., Ballardini, E., Bisceglia, M., Cinquetti, M., Brazzoduro, E., et al. Prophylactic use of a probiotic in the prevention of colic, regurgitation, and functional constipation: a randomized clinical trial. JAMA Pediatr. 168 (2014), 228–233.
41. Jiang, Y.H., Ehlers, M.D., Modeling autism by SHANK gene mutations in mice. Neuron 78 (2013), 8–27.
42. + tf/J mouse model of autism. PLoS ONE, 8, 2013, e61829.
43. Joyner, K., Smith, G.P., Gibbs, J., Abdominal vagotomy decreases the satiating potency of CCK-8 in sham and real feeding. Am. J. Physiol. 264 (1993), R912–R916.
44. Julio-Pieper, M., Bravo, J.A., Aliaga, E., Gotteland, M., Review article: intestinal barrier dysfunction and central nervous system disorders—a controversial association. Aliment. Pharmacol. Ther. 40 (2014), 1187–1201.
45. Kaelberer, M.M., Buchanan, K.L., Klein, M.E., Barth, B.B., Montoya, M.M., Shen, X., Bohórquez, D.V., A gut-brain neural circuit for nutrient sensory transduction. Science, 361, 2018, eaat5236.
46. Kawa, R., Saemundsen, E., Lóa Jónsdóttir, S., Hellendoorn, A., Lemcke, S., Canal-Bedia, R., García-Primo, P., Moilanen, I., European studies on prevalence and risk of autism spectrum disorders according to immigrant status-a review. Eur. J. Public Health 27 (2017), 101–110.
47. Kim, Y.S., Leventhal, B.L., Genetic epidemiology and insights into interactive genetic and environmental effects in autism spectrum disorders. Biol. Psychiatry 77 (2015), 66–74.
48. Kim, J.-W., Seung, H., Kim, K.C., Gonzales, E.L.T., Oh, H.A., Yang, S.M., Ko, M.J., Han, S.-H., Banerjee, S., Shin, C.Y., Agmatine rescues autistic behaviors in the valproic acid-induced animal model of autism. Neuropharmacology 113:Pt A (2017), 71–81.
49. Leclercq, S., Mian, F.M., Stanisz, A.M., Bindels, L.B., Cambier, E., Ben-Amram, H., Koren, O., Forsythe, P., Bienenstock, J., Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior. Nat. Commun., 8, 2017, 15062.
50. Lee, H.-J., Caldwell, H.K., Macbeth, A.H., Tolu, S.G., Young, W.S. 3rd, A conditional knockout mouse line of the oxytocin receptor. Endocrinology 149 (2008), 3256–3263.
51. Leng, G., Ludwig, M., Intranasal oxytocin: myths and delusions. Biol. Psychiatry 79 (2016), 243–250.
52. Lim, J.S., Lim, M.Y., Choi, Y., Ko, G., Modeling environmental risk factors of autism in mice induces IBD-related gut microbial dysbiosis and hyperserotonemia. Mol. Brain, 10, 2017, 14.
53. LoParo, D., Waldman, I.D., The oxytocin receptor gene (OXTR) is associated with autism spectrum disorder: a meta-analysis. Mol. Psychiatry 20 (2015), 640–646.
54. Mayer, E.A., Padua, D., Tillisch, K., Altered brain-gut axis in autism: comorbidity or causative mechanisms?. BioEssays 36 (2014), 933–939.
55. McElhanon, B.O., McCracken, C., Karpen, S., Sharp, W.G., Gastrointestinal symptoms in autism spectrum disorder: a meta-analysis. Pediatrics 133 (2014), 872–883.
56. McFarlane, H.G., Kusek, G.K., Yang, M., Phoenix, J.L., Bolivar, V.J., Crawley, J.N., Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 7 (2008), 152–163.
57. McMurdie, P.J., Holmes, S., phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8, 2013, e61217.
58. Melis, M.R., Melis, T., Cocco, C., Succu, S., Sanna, F., Pillolla, G., Boi, A., Ferri, G.L., Argiolas, A., Oxytocin injected into the ventral tegmental area induces penile erection and increases extracellular dopamine in the nucleus accumbens and paraventricular nucleus of the hypothalamus of male rats. Eur. J. Neurosci. 26 (2007), 1026–1035.
59. Methé B.A., Nelson, K.E., Pop, M., Creasy, H.H., Giglio, M.G., Huttenhower, C., Gevers, D., Petrosino, J.F., Abubucker, S., Badger, J.H., et al., Human Microbiome Project Consortium. A framework for human microbiome research. Nature 486 (2012), 215–221.
60. Meyza, K.Z., Blanchard, D.C., The BTBR mouse model of idiopathic autism - Current view on mechanisms. Neurosci. Biobehav. Rev. 76:Pt A (2017), 99–110.
61. Neufeld, K.M., Kang, N., Bienenstock, J., Foster, J.A., Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 23 (2011), 255–264.
62. Neumann, I.D., Maloumby, R., Beiderbeck, D.I., Lukas, M., Landgraf, R., Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology 38 (2013), 1985–1993.
63. Olson, C.A., Vuong, H.E., Yano, J.M., Liang, Q.Y., Nusbaum, D.J., Hsiao, E.Y., The gut microbiota mediates the anti-seizure effects of the ketogenic diet. Cell 173 (2018), 1728–1741.
64. Ornoy, A., Valproic acid in pregnancy: how much are we endangering the embryo and fetus?. Reprod. Toxicol. 28 (2009), 1–10.
65. Owyang, C., Heldsinger, A., Vagal control of satiety and hormonal regulation of appetite. J. Neurogastroenterol. Motil. 17 (2011), 338–348.
66. Peça, J., Feliciano, C., Ting, J.T., Wang, W., Wells, M.F., Venkatraman, T.N., Lascola, C.D., Fu, Z., Feng, G., Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472 (2011), 437–442.
67. Pedersen, C.A., Caldwell, J.D., Walker, C., Ayers, G., Mason, G.A., Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 108 (1994), 1163–1171.
68. Peñagarikano, O., Lázaro, M.T., Lu, X.H., Gordon, A., Dong, H., Lam, H.A., Peles, E., Maidment, N.T., Murphy, N.P., Yang, X.W., et al. Exogenous and evoked oxytocin restores social behavior in the Cntnap2 mouse model of autism. Sci. Transl. Med., 7, 2015, 271ra8.
69. Perez-Burgos, A., Wang, B., Mao, Y.-K., Mistry, B., McVey Neufeld, K.A., Bienenstock, J., Kunze, W., Psychoactive bacteria Lactobacillus rhamnosus (JB-1) elicits rapid frequency facilitation in vagal afferents. Am. J. Physiol. Gastrointest. Liver Physiol. 304 (2013), G211–G220.
70. Perez-Burgos, A., Mao, Y.-K., Bienenstock, J., Kunze, W.A., The gut-brain axis rewired: adding a functional vagal nicotinic “sensory synapse”. FASEB J. 28 (2014), 3064–3074.
71. Poutahidis, T., Kearney, S.M., Levkovich, T., Qi, P., Varian, B.J., Lakritz, J.R., Ibrahim, Y.M., Chatzigiagkos, A., Alm, E.J., Erdman, S.E., Microbial symbionts accelerate wound healing via the neuropeptide hormone oxytocin. PLoS ONE, 8, 2013, e78898.
72. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41 (2013), D590–D596.
73. Robinson, C., Schumann, R., Zhang, P., Young, R.C., Oxytocin-induced desensitization of the oxytocin receptor. Am. J. Obstet. Gynecol. 188 (2003), 497–502.
74. Sabatier, N., Leng, G., Menzies, J., Oxytocin, feeding, and satiety. Front. Endocrinol. (Lausanne), 4, 2013, 35.
75. Scattoni, M.L., Gandhy, S.U., Ricceri, L., Crawley, J.N., Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS ONE, 3, 2008, e3067.
76. Schieve, L.A., Gonzalez, V., Boulet, S.L., Visser, S.N., Rice, C.E., Van Naarden Braun, K., Boyle, C.A., Concurrent medical conditions and health care use and needs among children with learning and behavioral developmental disabilities, National Health Interview Survey, 2006-2010. Res. Dev. Disabil. 33 (2012), 467–476.
77. Sellaro, R., de Gelder, B., Finisguerra, A., Colzato, L.S., Transcutaneous vagus nerve stimulation (tVNS) enhances recognition of emotions in faces but not bodies. Cortex 99 (2018), 213–223.
78. Sharon, G., Sampson, T.R., Geschwind, D.H., Mazmanian, S.K., The central nervous system and the gut microbiome. Cell 167 (2016), 915–932.
79. Silverman, J.L., Yang, M., Lord, C., Crawley, J.N., Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 11 (2010), 490–502.
80. Stappenbeck, T.S., Virgin, H.W., Accounting for reciprocal host-microbiome interactions in experimental science. Nature 534 (2016), 191–199.
81. Stock, S., Uvnäs-Moberg, K., Increased plasma levels of oxytocin in response to afferent electrical stimulation of the sciatic and vagal nerves and in response to touch and pinch in anaesthetized rats. Acta Physiol. Scand. 132 (1988), 29–34.
82. Strati, F., Cavalieri, D., Albanese, D., De Felice, C., Donati, C., Hayek, J., Jousson, O., Leoncini, S., Renzi, D., Calabrò A., De Filippo, C., New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome, 5, 2017, 24.
83. Sullivan, E.L., Nousen, E.K., Chamlou, K.A., Maternal high fat diet consumption during the perinatal period programs offspring behavior. Physiol. Behav. 123 (2014), 236–242.
84. Sun, J., Qiao, Y., Qi, C., Jiang, W., Xiao, H., Shi, Y., Le, G.W., High-fat-diet-induced obesity is associated with decreased antiinflammatory Lactobacillus reuteri sensitive to oxidative stress in mouse Peyer's patches. Nutrition 32 (2016), 265–272.
85. Suzuki, T., Regulation of intestinal epithelial permeability by tight junctions. Cell. Mol. Life Sci. 70 (2013), 631–659.
86. Tabouy, L., Getselter, D., Ziv, O., Karpuj, M., Tabouy, T., Lukic, I., Maayouf, R., Werbner, N., Ben-Amram, H., Nuriel-Ohayon, M., et al. Dysbiosis of microbiome and probiotic treatment in a genetic model of autism spectrum disorders. Brain Behav. Immun. 73 (2018), 310–319.
87. Tang, Y., Chen, Z., Tao, H., Li, C., Zhang, X., Tang, A., Liu, Y., Oxytocin activation of neurons in ventral tegmental area and interfascicular nucleus of mouse midbrain. Neuropharmacology 77 (2014), 277–284.
88. Tomova, A., Husarova, V., Lakatosova, S., Bakos, J., Vlkova, B., Babinska, K., Ostatnikova, D., Gastrointestinal microbiota in children with autism in Slovakia. Physiol. Behav. 138 (2015), 179–187.
89. Tyzio, R., Nardou, R., Ferrari, D.C., Tsintsadze, T., Shahrokhi, A., Eftekhari, S., Khalilov, I., Tsintsadze, V., Brouchoud, C., Chazal, G., et al. Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343 (2014), 675–679.
90. Ungless, M.A., Whistler, J.L., Malenka, R.C., Bonci, A., Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411 (2001), 583–587.
91. Uvnäs-Moberg, K., Handlin, L., Petersson, M., Self-soothing behaviors with particular reference to oxytocin release induced by non-noxious sensory stimulation. Front. Psychol., 5, 2015, 1529.
92. Vuong, H.E., Hsiao, E.Y., Emerging roles for the gut microbiome in autism spectrum disorder. Biol. Psychiatry 81 (2017), 411–423.
93. Vuong, H.E., Yano, J.M., Fung, T.C., Hsiao, E.Y., The microbiome and host behavior. Annu. Rev. Neurosci. 40 (2017), 21–49.
94. Wang, X., Wang, B.R., Zhang, X.J., Xu, Z., Ding, Y.Q., Ju, G., Evidences for vagus nerve in maintenance of immune balance and transmission of immune information from gut to brain in STM-infected rats. World J. Gastroenterol. 8 (2002), 540–545.
95. Xiao, L., Priest, M.F., Nasenbeny, J., Lu, T., Kozorovitskiy, Y., Biased oxytocinergic modulation of midbrain dopamine systems. Neuron 95 (2017), 368–384.e5.
96. Yang, M., Crawley, J.N., Simple behavioral assessment of mouse olfaction. Curr. Protoc. Neurosci. 48 (2009), 8.24.21–28.24.12.
97. Yang, M., Perry, K., Weber, M.D., Katz, A.M., Crawley, J.N., Social peers rescue autism-relevant sociability deficits in adolescent mice. Autism Res. 4 (2011), 17–27.
98. Zhang, T.A., Placzek, A.N., Dani, J.A., In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology 59 (2010), 431–436.
99. Zhang, Q., Widmer, G., Tzipori, S., A pig model of the human gastrointestinal tract. Gut Microbes 4 (2013), 193–200.
100. Zhang, M., Ma, W., Zhang, J., He, Y., Wang, J., Analysis of gut microbiota profiles and microbe-disease associations in children with autism spectrum disorders in China. Sci. Rep., 8, 2018, 13981.
101. Zhao, H., Tu, Z., Xu, H., Yan, S., Yan, H., Zheng, Y., Yang, W., Zheng, J., Li, Z., Tian, R., et al. Altered neurogenesis and disrupted expression of synaptic proteins in prefrontal cortex of SHANK3-deficient non-human primate. Cell Res. 27 (2017), 1293–1297.