The effects of gut microbiota on CNS function in humans

Gut Microbes

Volumn 5, Issue 3, 2014, Pages 404-410

  Tillisch, Kirsten ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anxiety; Brain gut axis; Depression; Microbiota; Probiotic

Indexed keywords

ANXIETY ASSESSMENT; ARTICLE; BEHAVIOR CHANGE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BREAST FEEDING; CAMPYLOBACTER JEJUNI; CENTRAL NERVOUS SYSTEM FUNCTION; DISEASE TRANSMISSION; ENVIRONMENTAL FACTOR; EPIGENETICS; HUMAN; INTESTINE FLORA; NONHUMAN; SIGNAL TRANSDUCTION; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASE; GASTROINTESTINAL TRACT; MICROBIOLOGY; MICROFLORA; PATHOPHYSIOLOGY; PHYSIOLOGY;

CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASES; GASTROINTESTINAL TRACT; HUMANS; MICROBIOTA;

EID: 84964315352     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.29232     Document Type: Article

References (77)

1. Jiménez E, Fernández L, Marín ML, Martín R, Odriozola JM, Nueno-Palop C, Narbad A, Olivares M, Xaus J, Rodríguez JM. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 2005; 51: 270-4; PMID: 16187156; http://dx.doi.org/10.1007/s00284-005-0020-3
2. Wagner CL, Taylor SN, Johnson D. Host factors in amniotic fluid and breast milk that contribute to gut maturation. Clin Rev Allergy Immunol 2008; 34: 191-204; PMID: 18330727; http://dx.doi.org/10.1007/s12016-007-8032-3
3. Satokari R, Grönroos T, Laitinen K, Salminen S, Isolauri E. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 2009; 48: 8-12; PMID: 19018955; http://dx.doi.org/10.1111/j.1472-765X.2008.02475.x
4. Al-Asmakh M, Anuar F, Zadjali F, Rafter J, Pettersson S. Gut microbial communities modulating brain development and function. Gut Microbes 2012; 3: 366-73; PMID: 22743758; http://dx.doi.org/10.4161/gmic.21287
5. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL; CHILD Study Investigators. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 2013; 185: 385-94; PMID: 23401405; http://dx.doi.org/10.1503/cmaj.121189
6. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006; 118: 511-21; PMID: 16882802; http://dx.doi.org/10.1542/peds.2005-2824
7. Butel MJ, Suau A, Campeotto F, Magne F, Aires J, Ferraris L, Kalach N, Leroux B, Dupont C. Conditions of bifidobacterial colonization in preterm infants: a prospective analysis. J Pediatr Gastroenterol Nutr 2007; 44: 577-82; PMID: 17460489; http://dx.doi.org/10.1097/MPG.0b013e3180406b20
8. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 2011; 108(SUPPL 1): 4578-85; PMID: 20668239; http://dx.doi.org/10.1073/pnas.1000081107
9. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature 2012; 486: 222-7; PMID: 22699611
10. Mischke M, Plösch T. More than just a gut instinctthe potential interplay between a baby’s nutrition, its gut microbiome, and the epigenome. Am J Physiol Regul Integr Comp Physiol 2013; 304: R1065-9; PMID: 23594611; http://dx.doi.org/10.1152/ajpregu.00551.2012
11. Weaver IC. Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let’s call the whole thing off. Epigenetics 2007; 2: 22-8; PMID: 17965624; http://dx.doi.org/10.4161/epi.2.1.3881
12. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, Kubo C, Koga Y. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558: 263-75; PMID: 15133062; http://dx.doi.org/10.1113/jphysiol.2004.063388
13. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108: 3047-52; PMID: 21282636; http://dx.doi.org/10.1073/pnas.1010529108
14. Holmes E, Kinross J, Gibson GR, Burcelin R, Jia W, Pettersson S, Nicholson JK. Therapeutic modulation of microbiota-host metabolic interactions. Sci Transl Med 2012; 4: rv6; 8; http://dx.doi.org/10.1126/scitranslmed.3004244
15. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science 2012; 336: 1262-7; PMID: 22674330; http://dx.doi.org/10.1126/science.1223813
16. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 2012; 10: 735-42; PMID: 23000955; http://dx.doi.org/10.1038/nrmicro2876
17. Montiel-Castro AJ, González-Cervantes RM, Bravo-Ruiseco G, Pacheco-López G. The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front Integr Neurosci 2013; 7: 70; PMID: 24109440; http://dx.doi.org/10.3389/fnint.2013.00070
18. Berntson GG, Sarter M, Cacioppo JT. Ascending visceral regulation of cortical affective information processing. Eur J Neurosci 2003; 18: 2103-9; PMID: 14622171; http://d.doi.org/10.1046/j.1460-9568.2003.02967.x
19. Lyte M, Varcoe JJ, Bailey MT. Anxiogenic effect of subclinical bacterial infection in mice in the absence of overt immune activation. Physiol Behav 1998; 65: 63-8; PMID: 9811366; http://dx.doi.org/10.1016/S0031-9384(98)00145-0
20. Marshall JK, Thabane M, Garg AX, Clark WF, Salvadori M, Collins SM; Walkerton Health Study Investigators. Incidence and epidemiology of irritable bowel syndrome after a large waterborne outbreak of bacterial dysentery. Gastroenterology 2006; 131: 445-50, quiz 660; PMID: 16890598; http://dx.doi.org/10.1053/j.gastro.2006.05.053
21. Goehler LE, Gaykema RP, Opitz N, Reddaway R, Badr N, Lyte M. Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 2005; 19: 334-44; PMID: 15944073; http://dx.doi.org/10.1016/j.bbi.2004.09.002
22. Goehler LE, Park SM, Opitz N, Lyte M, Gaykema RP. Campylobacter jejuni infection increases anxietylike behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 2008; 22: 354-66; PMID: 17920243; http://dx.doi.org/10.1016/j.bbi.2007.08.009
23. Gaykema RP, Goehler LE, Lyte M. Brain response to cecal infection with Campylobacter jejuni: analysis with Fos immunohistochemistry. Brain Behav Immun 2004; 18: 238-45; PMID: 15050651; http://dx.doi.org/10.1016/j.bbi.2003.08.002
24. Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, Deng Y, Blennerhassett PA, Fahnestock M, Moine D, et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gutbrain communication. Neurogastroenterol Motil 2011; 23: 1132-9; PMID: 21988661; http://dx.doi.org/10.1111/j.1365-2982.2011.01796.x
25. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108: 3047-52; PMID: 21282636; http://dx.doi.org/10.1073/pnas.1010529108
26. Holmes E, Kinross J, Gibson GR, Burcelin R, Jia W, Pettersson S, Nicholson JK. Therapeutic modulation of microbiota-host metabolic interactions. Sci Transl Med 2012; 4: rv6; PMID: 22674556; http://dx.doi.org/10.1126/scitranslmed.3004244
27. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science 2012; 336: 1262-7; PMID: 22674330; http://dx.doi.org/10.1126/science.1223813
28. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 2012; 10: 735-42; PMID: 23000955; http://dx.doi.org/10.1038/nrmicro2876
29. Montiel-Castro AJ, González-Cervantes RM, Bravo-Ruiseco G, Pacheco-López G. The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front Integr Neurosci 2013; 7: 70; PMID: 24109440; http://dx.doi.org/10.3389/fnint.2013.00070
30. Berntson GG, Sarter M, Cacioppo JT. Ascending visceral regulation of cortical affective information processing. Eur J Neurosci 2003; 18: 2103-9; PMID: 14622171; http://dx.doi.org/10.1046/j.1460-9568.2003.02967.x
31. Lyte M, Varcoe JJ, Bailey MT. Anxiogenic effect of subclinical bacterial infection in mice in the absence of overt immune activation. Physiol Behav 1998; 65: 63-8; PMID: 9811366; http://dx.doi.org/10.1016/S0031-9384(98)00145-0
32. Marshall JK, Thabane M, Garg AX, Clark WF, Salvadori M, Collins SM; Walkerton Health Study Investigators. Incidence and epidemiology of irritable bowel syndrome after a large waterborne outbreak of bacterial dysentery. Gastroenterology 2006; 131: 445-50, quiz 660; PMID: 16890598; http://dx.doi.org/10.1053/j.gastro.2006.05.053
33. Goehler LE, Gaykema RP, Opitz N, Reddaway R, Badr N, Lyte M. Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 2005; 19: 334-44; PMID: 15944073; http://dx.doi.org/10.1016/j.bbi.2004.09.002
34. Goehler LE, Park SM, Opitz N, Lyte M, Gaykema RP. Campylobacter jejuni infection increases anxietylike behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 2008; 22: 354-66; PMID: 17920243; http://dx.doi.org/10.1016/j.bbi.2007.08.009
35. Gaykema RP, Goehler LE, Lyte M. Brain response to cecal infection with Campylobacter jejuni: analysis with Fos immunohistochemistry. Brain Behav Immun 2004; 18: 238-45; PMID: 15050651; http://dx.doi.org/10.1016/j.bbi.2003.08.002
36. Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, Deng Y, Blennerhassett PA, Fahnestock M, Moine D, et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gutbrain communication. Neurogastroenterol Motil 2011; 23: 1132-9; PMID: 21988661; http://dx.doi.org/10.1111/j.1365-2982.2011.01796.x
37. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson JF, Rougeot C, Pichelin M, Cazaubiel M, et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 2011; 105: 755-64; PMID: 20974015; http://dx.doi.org/10.1017/S0007114510004319
38. Messaoudi M, Violle N, Bisson JF, Desor D, Javelot H, Rougeot C. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes 2011; 2: 256-61; PMID: 21983070; http://dx.doi.org/10.4161/gmic.2.4.16108
39. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, Britton RA, Kalkum M, Versalovic J. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 2012; 7: e31951; PMID: 22384111; http://dx.doi.org/10.1371/journal.pone.0031951
40. Asano Y, Hiramoto T, Nishino R, Aiba Y, Kimura T, Yoshihara K, Koga Y, Sudo N. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol 2012; 303: G1288-95; PMID: 23064760; http://dx.doi.org/10.1152/ajpgi.00341.2012
41. Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C. γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 2012; 113: 411-7; PMID: 22612585; http://dx.doi.org/10.1111/j.1365-2672.2012.05344.x
42. Uribe A, Alam M, Johansson O, Midtvedt T, Theodorsson E. Microflora modulates endocrine cells in the gastrointestinal mucosa of the rat. Gastroenterology 1994; 107: 1259-69; PMID: 7926490; http://dx.doi.org/10.1016/0016-5085(94)90526-6
43. Butterworth RF. The liver-brain axis in liver failure: neuroinflammation and encephalopathy. Nat Rev Gastroenterol Hepatol 2013; 10: 522-8; PMID: 23817325; http://dx.doi.org/10.1038/nrgastro.2013.99
44. Lesniewska V, Rowland I, Cani PD, Neyrinck AM, Delzenne NM, Naughton PJ. Effect on components of the intestinal microflora and plasma neuropeptide levels of feeding Lactobacillus delbrueckii, Bifidobacterium lactis, and inulin to adult and elderly rats. Appl Environ Microbiol 2006; 72: 6533-8; PMID: 17021202; http://dx.doi.org/10.1128/AEM.00915-06
45. Holmes E, Li JV, Marchesi JR, Nicholson JK. Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab 2012; 16: 559-64; PMID: 23140640; http://dx.doi.org/10.1016/j.cmet.2012.10.007
46. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J Psychiatr Res 2008; 43: 164-74; PMID: 18456279; http://dx.doi.org/10.1016/j.jpsychires.2008.03.009
47. Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, Hammer RE, Williams SC, Crowley J, Yanagisawa M, et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A 2008; 105: 16767-72; PMID: 18931303; http://dx.doi.org/10.1073/pnas.0808567105
48. Duca FA, Swartz TD, Sakar Y, Covasa M. Increased oral detection, but decreased intestinal signaling for fats in mice lacking gut microbiota. PLoS One 2012; 7: e39748; PMID: 22768116; http://dx.doi.org/10.1371/journal.pone.0039748
49. Martin FP, Rezzi S, Peré-Trepat E, Kamlage B, Collino S, Leibold E, Kastler J, Rein D, Fay LB, Kochhar S. Metabolic effects of dark chocolate consumption on energy, gut microbiota, and stressrelated metabolism in free-living subjects. J Proteome Res 2009; 8: 5568-79; PMID: 19810704; http://dx.doi.org/10.1021/pr900607v
50. Pase MP, Scholey AB, Pipingas A, Kras M, Nolidin K, Gibbs A, Wesnes K, Stough C. Cocoa polyphenols enhance positive mood states but not cognitive performance: a randomized, placebo-controlled trial. J Psychopharmacol 2013; 27: 451-8; PMID: 23364814; http://dx.doi.org/10.1177/0269881112473791
51. Parker G, Parker I, Brotchie H. Mood state effects of chocolate. J Affect Disord 2006; 92: 149-59; PMID: 16546266; http://dx.doi.org/10.1016/j.jad.2006.02.007
52. Guyonnet D, Schlumberger A, Mhamdi L, Jakob S, Chassany O. Fermented milk containing Bifidobacterium lactis DN-173 010 improves gastrointestinal well-being and digestive symptoms in women reporting minor digestive symptoms: a randomised, double-blind, parallel, controlled study. Br J Nutr 2009; 102: 1654-62; PMID: 19622191; http://dx.doi.org/10.1017/S0007114509990882
53. Marteau P, Guyonnet D, Lafaye de Micheaux P, Gelu S. A randomized, double-blind, controlled study and pooled analysis of two identical trials of fermented milk containing probiotic Bifidobacterium lactis CNCM I-2494 in healthy women reporting minor digestive symptoms. Neurogastroenterol Motil 2013; 25: 331-e252; PMID: 23480238; http://dx.doi.org/10.1111/nmo.12078
54. Whorwell PJ, Altringer L, Morel J, Bond Y, Charbonneau D, O’Mahony L, Kiely B, Shanahan F, Quigley EM. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am J Gastroenterol 2006; 101: 1581-90; PMID: 16863564; http://dx.doi.org/10.1111/j.1572-0241.2006.00734.x
55. Pimentel M, Lembo A, Chey WD, Zakko S, Ringel Y, Yu J, Mareya SM, Shaw AL, Bortey E, Forbes WP; TARGET Study Group. Rifaximin therapy for patients with irritable bowel syndrome without constipation. N Engl J Med 2011; 364: 22-32; PMID: 21208106; http://dx.doi.org/10.1056/NEJMoa1004409
56. Benedetti F, Mayberg HS, Wager TD, Stohler CS, Zubieta JK. Neurobiological mechanisms of the placebo effect. J Neurosci 2005; 25: 10390-402; PMID: 16280578; http://dx.doi.org/10.1523/JNEUROSCI.3458-05.2005
57. Keita AV, Söderholm JD. The intestinal barrier and its regulation by neuroimmune factors. Neurogastroenterol Motil 2010; 22: 718-33; PMID: 20377785; http://dx.doi.org/10.1111/j.1365-2982.2010.01498.x
58. Schreiber KL, Brown DR. Adrenocorticotrophic hormone modulates Escherichia coli O157: H7 adherence to porcine colonic mucosa. Stress 2005; 8: 185-90; PMID: 16329163; http://dx.doi.org/10.1080/10253890500188732
59. Spitz J, Hecht G, Taveras M, Aoys E, Alverdy J. The effect of dexamethasone administration on rat intestinal permeability: the role of bacterial adherence. Gastroenterology 1994; 106: 35-41; PMID: 8276206
60. Unsal H, Balkaya M, Unsal C, Biyik H, Basbülbül G, Poyrazoglu E. The short-term effects of different doses of dexamethasone on the numbers of some bacteria in the ileum. Dig Dis Sci 2008; 53: 1842-5; PMID: 18049898; http://dx.doi.org/10.1007/s10620-007-0089-6
61. Bailey MT, Coe CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 1999; 35: 146-55; PMID: 10461128; http://dx.doi.org/10.1002/(SICI)1098-2302(199909)35:2<146::AIDDEV7>3.0.CO;2-G
62. Bailey MT, Lubach GR, Coe CL. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 2004; 38: 414-21; PMID: 15085020; http://dx.doi.org/10.1097/00005176-200404000-00009
63. O’Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009; 65: 263-7; PMID: 18723164; http://dx.doi.org/10.1016/j.biopsych.2008.06.026
64. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 2010; 78: 1509-19; PMID: 20145094; http://dx.doi.org/10.1128/IAI.00862-09
65. Sandler RH, Finegold SM, Bolte ER, Buchanan CP, Maxwell AP, Väisänen ML, Nelson MN, Wexler HM. Short-term benefit from oral vancomycin treatment of regressive-onset autism. J Child Neurol 2000; 15: 429-35; PMID: 10921511; http://dx.doi.org/10.1177/088307380001500701
66. Ming X, Stein TP, Barnes V, Rhodes N, Guo L. Metabolic perturbance in autism spectrum disorders: a metabolomics study. J Proteome Res 2012; 11: 5856-62; PMID: 23106572
67. De Angelis M, Piccolo M, Vannini L, Siragusa S, De Giacomo A, Serrazzanetti DI, Cristofori F, Guerzoni ME, Gobbetti M, Francavilla R. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS One 2013; 8: e76993; PMID: 24130822; http://dx.doi.org/10.1371/journal.pone.0076993
68. Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, Youn E, Summanen PH, Granpeesheh D, Dixon D, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010; 16: 444-53; PMID: 20603222; http://dx.doi.org/10.1016/j.anaerobe.2010.06.008
69. Finegold SM, Molitoris D, Song Y, Liu C, Vaisanen ML, Bolte E, McTeague M, Sandler R, Wexler H, Marlowe EM, et al. Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis 2002; 35(SUPPL 1): S6-16; PMID: 12173102; http://dx.doi.org/10.1086/341914
70. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013; 155: 1451-63; PMID: 24315484; http://dx.doi.org/10.1016/j.cell.2013.11.024
71. Brenner SR. Blue-green algae or cyanobacteria in the intestinal micro-flora may produce neurotoxins such as Beta-N-Methylamino-L-Alanine (BMAA) which may be related to development of amyotrophic lateral sclerosis, Alzheimer’s disease and Parkinson-Dementia-Complex in humans and Equine Motor Neuron Disease in horses. Med Hypotheses 2013; 80: 103; PMID: 23146671; http://dx.doi.org/10.1016/j.mehy.2012.10.010
72. Ohland CL, Kish L, Bell H, Thiesen A, Hotte N, Pankiv E, Madsen KL. Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology 2013; 38: 1738-47; PMID: 23566632; http://dx.doi.org/10.1016/j.psyneuen.2013.02.008
73. Davari S, Talaei SA, Alaei H, Salami M. Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiomegut-brain axis. Neuroscience 2013; 240: 287-96; PMID: 23500100; http://dx.doi.org/10.1016/j.neuroscience.2013.02.055
74. Foster JA, McVey Neufeld KA. Gut-brain axis: how the microbiome influences anxiety and depression.Trends Neurosci 2013; 36: 305-12; PMID: 23384445; http://dx.doi.org/10.1016/j.tins.2013.01.005
75. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 2011; 108: 16050-5; PMID: 21876150; http://dx.doi.org/10.1073/pnas.1102999108
76. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170: 1179-88; PMID: 20696216; http://dx.doi.org/10.1016/j.neuroscience.2010.08.005
77. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, Guyonnet D, Legrain-Raspaud S, Trotin B, Naliboff B, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 2013; 144: 1394-401, e1-4; PMID: 23474283; http://dx.doi.org/10.1053/j.gastro.2013.02.043