Neurobehavioural effects of Lactobacillus rhamnosus GG alone and in combination with prebiotics polydextrose and galactooligosaccharide in male rats exposed to early-life stress

References

• Andersen SL. Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 2003;27:3–18. doi: 10.1016/S0149-7634(03)00005-8
   PubMed Web of Science ®Google Scholar
• Borre YE, O’Keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JC. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med 2014;20(9):509–18. doi: 10.1016/j.molmed.2014.05.002
   PubMed Web of Science ®Google Scholar
• Huttenlocher PR. Synaptic density in human frontal cortex – developmental changes and effects of aging. Brain Res 1979;163:195–205. doi: 10.1016/0006-8993(79)90349-4
   PubMed Web of Science ®Google Scholar
• Petanjek Z, Judas M, Simic G, Rasin MR, Uylings HB, Rakic P et al. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci USA 2011;108:13281–6. doi: 10.1073/pnas.1105108108
   PubMed Web of Science ®Google Scholar
• Schmidt M, Enthoven L, van der Mark M, Levine S, de Kloet ER, Oitzl MS. Postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. Int J Dev Neurosci. 2003;21:125–32. doi: 10.1016/S0736-5748(03)00030-3
   PubMed Web of Science ®Google Scholar
• McVey Neufeld KA, Luczynski P, Dinan TG, Cryan JF. Reframing the teenage wasteland: adolescent microbiota-gut-brain axis. Cdn J Psych 2016. 61(4):214–21
   Google Scholar
• Coplan JD, Andrews MW, Rosenblum LA, Owens MJ, Friedman S, Gorman JM, et al. Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proc Natl Acad Sci USA 1996;93:1619–23. doi: 10.1073/pnas.93.4.1619
   PubMed Web of Science ®Google Scholar
• Kaplow JB, Widom CS. Age of onset of child maltreatment predicts long-term mental health outcomes. J Abnorm Psychol 2007;116:176–87. doi: 10.1037/0021-843X.116.1.176
   PubMed Web of Science ®Google Scholar
• Cryan JF, Dinan TG. Unraveling the longstanding scars of early neurodevelopmental stress. Biol Psychiatry 2013;74:788–9. doi: 10.1016/j.biopsych.2013.10.004
   PubMed Web of Science ®Google Scholar
• Hulshof HJ, Novati A, Sgoifo A, Luiten PG, den Boer JA, Meerlo P. Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effects on stress sensitivity and anxiety in adult wistar rats. Behav Brain Res 2011;216:552–60. doi: 10.1016/j.bbr.2010.08.038
   PubMed Web of Science ®Google Scholar
• O’Mahony SM, Hyland NP, Dinan TG, Cryan JF. Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl) 2011;214(1):71–88. doi: 10.1007/s00213-010-2010-9
   PubMed Web of Science ®Google Scholar
• O’Mahony SM, Clarke G, Dinan TG, Cryan JF. Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle? Neuroscience. 2017a;342:37–54. doi: 10.1016/j.neuroscience.2015.09.068
   PubMed Web of Science ®Google Scholar
• Maccari S, Krugers HJ, Morley-Fletcher S, Szyf M, Brunton PJ. The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations. J Neuroendocrinol 2014;26:707–23 doi: 10.1111/jne.12175
   PubMed Web of Science ®Google Scholar
• O’Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho A-M, Quigley EMM, et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illness. Biol Psychiatry 2009;65:263-67. doi: 10.1016/j.biopsych.2008.06.026
   PubMed Web of Science ®Google Scholar
• Moloney RD, O’Leary OF, Felice D, Bettler B, Dinan TG, Cryan JF. Early-life stress induces visceral hypersensitivity in mice. Neurosci Lett. 2012;512(2):99–102. doi: 10.1016/j.neulet.2012.01.066
   PubMed Web of Science ®Google Scholar
• Hyland NP, O’Mahony SM, O’Malley D, O’Mahony CM, Dinan TG, Cryan JF. Early-life stress selectively affects gastrointestinal but not behavioural responses in a genetic model of brain-gut axis dysfunction. Neurogastroenterol Motil 2015;27:105–13. doi: 10.1111/nmo.12486
   PubMed Web of Science ®Google Scholar
• Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol. 2009;6(5):306–14. doi: 10.1038/nrgastro.2009.35
   PubMed Web of Science ®Google Scholar
• Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behavior. Nat Rev Neurosci 2012;13(10):701–12. doi: 10.1038/nrn3346
   PubMed Web of Science ®Google Scholar
• Jeffery IB, Quigley EM, Ohman L, Simren M, O’Toole PW. The microbiota link to irritable bowel syndrome: an emerging story. Gut Microbes 2012;3(6):572–6. doi: 10.4161/gmic.21772
   PubMed Web of Science ®Google Scholar
• McVey Neufeld KA, Foster JA. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 2013;36(5):305–12 doi: 10.1016/j.tins.2013.01.005
   PubMed Web of Science ®Google Scholar
• Collins SM. A role for the gut microbiota in IBS. Nat Rev Gastroenterol Hepatol 2014;11(8):497–505. doi: 10.1038/nrgastro.2014.40
   PubMed Web of Science ®Google Scholar
• De Palma G, Collins SM, Bercik P, Verdu EF. The microbiota-gut-brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both? J Physiol 2014;592(Pt 14):2989–97. doi: 10.1113/jphysiol.2014.273995
   PubMed Web of Science ®Google Scholar
• Mayer EA, Padua D, Tillisch K. Altered brain-gut axis in autism: comorbidity or causative mechanisms? Bioessays 2014;36(10):933–9. doi: 10.1002/bies.201400075
   PubMed Web of Science ®Google Scholar
• O’Mahony SM, Dinan TG., Cryan JF. The gut microbiota as a key regulator of visceral pain. Pain. 2017;158(Suppl 1):S19–S28. doi:10.1097/j.pain.0000000000000779.
   PubMed Web of Science ®Google Scholar
• Sandhu KV, Sherwin E, Schellekens H, Stanton C, Dinan TG, Cryan JF. Feeding the microbiota-gut-brain axis: diet, microbiome and neuropsychiatry. Transl Res 2016. doi:10.1016/j.trsl.2016.10.002.
   PubMed Web of Science ®Google Scholar
• Sanders ME, Guarner F, Guerrant R, Holt PR, Quigley EMM, Sartor RB, et al. An update on the use and investigation of probiotics in health and disease. Gut 2013;62(5):787–96. doi: 10.1136/gutjnl-2012-302504
   PubMed Web of Science ®Google Scholar
• 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. doi: 10.1016/j.neuroscience.2010.08.005
   PubMed Web of Science ®Google Scholar
• Suri D, Veenit V, Sarkar A, Thiagarajan D, Kumar A, Nestler EJ, et al. Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition. Biol Psychiatry 2013;73:658–66. doi: 10.1016/j.biopsych.2012.10.023
   PubMed Web of Science ®Google Scholar
• Suri D, Bhattacharya A, Vaidya VA. Early stress evokes temporally distinct consequences on the hippocampal transcriptome, anxiety and cognitive behavior. Int J Neuropsychopharmacol 2014;17:289–301. doi: 10.1017/S1461145713001004
   PubMed Web of Science ®Google Scholar
• Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 1995;125(6):1401–12. doi: 10.1093/jn/125.6.1401
   PubMed Web of Science ®Google Scholar
• Roberfroid M. Prebiotics: the concept revisited. J Nutr 2007;137(3 Suppl 2):830S–7S. doi: 10.1093/jn/137.3.830S
   PubMed Web of Science ®Google Scholar
• Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K, Clarke G, et al. Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry 2017;82(7):472–487. doi: 10.1016/j.biopsych.2016.12.031
   PubMed Web of Science ®Google Scholar
• Tarr AJ, Galley JD, Fisher SE, Chichlowski M, Berg BM, Bailey MT. The prebiotics 3’sialyllactose and 6’sialyllactose diminish stressor-induced anxiety-like behavior and colonic microbiota alterations: evidence for effects on the gut-brain axis. Brain Behav Immun 2015;50:166–77 doi: 10.1016/j.bbi.2015.06.025
   PubMed Web of Science ®Google Scholar
• Mika A, Day HED, Martinez A, Rumian NL, Greenwood BN, Chichlowski M, et al. Early life diets with prebiotics and bioactive milk fractions attenuate the impact of stress on learned helplessness behaviours and later gene expression within neural circuits important for stress resistance. Eur J Neurosci. 2016. doi:10.1111/ejn.13444.
   PubMed Web of Science ®Google Scholar
• Kannampalli P, Pochiraju S, Chichlowski M, Berg BM, Rudolph C, Brukert M et al. Probiotic Lactobacillus rhamnosus GG (LGG) and prebiotic prevent neonatal inflammation-induced visceral hypersensitivity in adult rats. Neurogastroenterol Motil 2014;12:1694–704. doi: 10.1111/nmo.12450
   Web of Science ®Google Scholar
• Neumann ID, Wigger A, Kromer S, Frank E, Landgraf R, Bosch OJ. Differential effects of periodic maternal separation on adult stress coping in rat models of extremes in trait anxiety. Neuroscience 2005;132:867–77. doi: 10.1016/j.neuroscience.2005.01.034
   PubMed Web of Science ®Google Scholar
• O’Mahony SM, Felice VD, Nally K, Savignac HM, Claesson MJ, Scully P, et al. Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive of anxiety-related behaviors in male rats. Neuroscience. 2014;277:885–901. doi: 10.1016/j.neuroscience.2014.07.054
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001;25(4):402–8 doi: 10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Stanford SC. The open field test: reinventing the wheel. J Psychopharmacol 2007;21:134–5. doi: 10.1177/0269881107073199
   PubMed Web of Science ®Google Scholar
• Bharwani A, Mian MF, Surette MG, Bienenstock J, Forsythe P. Oral treatment with Lactobacillus rhamnosus attenuates behavioural deficits and immune changes in chronic social stress. BMC Med 2017;15:7. doi: 10.1186/s12916-016-0771-7
   PubMed Web of Science ®Google Scholar
• Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006;1(2):848–58 doi: 10.1038/nprot.2006.116
   PubMed Web of Science ®Google Scholar
• Vorhees CV, Williams MT. Assessing spatial learning and memory in rodents. ILAR J 2014;55:310–32. doi: 10.1093/ilar/ilu013
   PubMed Web of Science ®Google Scholar
• Savignac HM, Tramullas M, Kiely B, Dinan TG, Cryan JF. Bifidobactera modulate cognitive processes in an anxious mouse strain. Behav Brain Res 2015;287:59–72. doi: 10.1016/j.bbr.2015.02.044
   PubMed Web of Science ®Google Scholar
• Hsu F-C, Zhang G-J, Raol YSH, Valentino RF, Coulter DA, Brooks-Kayal AR. Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioural stress response. Proc Natl Acad Sci USA 2003;100(21):12213–8. doi: 10.1073/pnas.2131679100
   PubMed Web of Science ®Google Scholar
• Jacobson-Pick S, Elkobi A, Vander S, Rosenblum K, Richter-Levin G. Juvenile stress-induced alteration of maturation of the GABAA receptor α subunit in the rat. Int J Neuropsychopharm 2011;11:891–903.
   Google Scholar
• Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 2011;108(38):16050–5. doi: 10.1073/pnas.1102999108
   PubMed Web of Science ®Google Scholar
• Janik R, Thomason LAM, Stanisz AM, Forsythe P, Bienenstock J, Stanisz GJ. Magnetic resonance spectroscopy reveals oral Lactobacillus promotion of increases in brain GABA, N-acetyl aspartate and glutamate. NeuroImage 2016;125:988–95. doi: 10.1016/j.neuroimage.2015.11.018
   PubMed Web of Science ®Google Scholar
• Lehner M, Wislowska-Stanek A, Skorzewska A, Maciejak P, Szyndler J, Turzynska D, et al. Differences in the density of the GABA-A receptor alpha-2 subunits and gephyrin in brain structures of rats selected for low and high anxiety in basal and fear-stimulated conditions, in a model of contextual fear conditioning. Neurobiol Learn Mem 2010;94(4):499–508. doi: 10.1016/j.nlm.2010.09.001
   PubMed Web of Science ®Google Scholar
• O’Leary OF, Felice D, Galimberti S, Savignac HM, Bravo JA, Crowley T, et al. Gabab(1) receptor subunit isoforms differentially regulate stress resilience. PNAS 2014;111(42):15232–7. doi: 10.1073/pnas.1404090111
   PubMed Web of Science ®Google Scholar
• Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Plotsky PM. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol Psychiatry 2004;55(4):367–75. doi: 10.1016/j.biopsych.2003.10.007
   PubMed Web of Science ®Google Scholar
• Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 2007;32:256–66. doi: 10.1016/j.psyneuen.2006.12.013
   PubMed Web of Science ®Google Scholar
• Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behavior and cognition. Nat Rev Neurosci 2009;10:434–45. doi: 10.1038/nrn2639
   PubMed Web of Science ®Google Scholar
• Nemoto, T, Kakinuma Y, Shibasaki T. Impaired miR449a-induced downregulation of Crhr1 expression in low-birth-weight rats. J Endocrinol. 2015;224:195–203. doi: 10.1530/JOE-14-0537
   PubMed Web of Science ®Google Scholar