Skip to main content
SpringerLink
Log in

Post-Weaning Treatment with Probiotic Inhibited Stress-Induced Amnesia in Adulthood Rats: The Mediation of GABAergic System and BDNF/c-Fos Signaling Pathways

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

The current study aimed to examine the effect of post-weaning treatment with probiotics on memory formation under stress during the adult period in male Wistar rats. Considering GABA is a potential mediator between probiotics and the host, the present study also investigated the involvement of the GABAergic system in the probiotic response. The hippocampal and prefrontal cortical (PFC) expression levels of BDNF and c-Fos were also assessed to show whether the treatments affect the memory-related signaling pathway. Three weeks after birth, the post-weaning rats were fed with probiotic water (PW) or tap water (TW) for 2, 3, 4, or 5 weeks. Exposure to acute stress impaired memory formation in a passive avoidance learning task. Feeding the post-weaning animals with probiotic strains (3, 4, or 5 weeks) inhibited stress-induced amnesia of the adult period. Post-training intracerebroventricular (ICV) microinjection of muscimol improved stress-induced amnesia in the animals fed with TW. ICV microinjection of muscimol inhibited probiotic treatment’s significant effect on the stress response in the memory task. The expression levels of BDNF and c-Fos in the PFC and the hippocampus were significantly decreased in the stress animal group. The levels of BDNF and c-Fos were increased in the PW/stress animal group. The muscimol response was compounded with the decreased levels of BDNF and c-Fos in the PFC and the hippocampus. Thus, the GABA-A receptor mechanism may mediate the inhibitory effect of this probiotic mixture on stress-induced amnesia, which may be associated with the PFC and hippocampal BDNF/c-Fos signaling changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The detailed data and all statistical analyses are available from the corresponding author upon request.

Abbreviations

BDNF:

Brain-derived neurotrophic factor

PFC:

Prefrontal cortex

ICV:

Intracerebroventricular

GABA:

Gamma-aminobutyric acid

TW:

Tap water

PW:

Probiotic water

ANOVA:

Analysis of variance

SEM:

Standard error of mean

References

  1. Dieterich W, Schink M, Zopf Y (2018) Microbiota in the gastrointestinal tract. Med Sci 6:116

    CAS  Google Scholar 

  2. Martin CR, Osadchiy V, Kalani A, Mayer EA (2018) The brain-gut-microbiome axis. Cell Mol Gastroenterol Hepatol 6:133–148

    Article  PubMed  PubMed Central  Google Scholar 

  3. Carabotti M, Scirocco A, Maselli MA, Severi C (2015) The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol 28:203

    PubMed  PubMed Central  Google Scholar 

  4. Roller M, Rechkemmer G, Watzl B (2004) Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr 134:153–156

    Article  CAS  PubMed  Google Scholar 

  5. Karamese M, Aydin H, Sengul E, Gelen V, Sevim C, Ustek D, Karakus E (2016) The immunostimulatory effect of lactic acid bacteria in a rat model. Iran J Immunol 13:220–228

    PubMed  Google Scholar 

  6. Weijun T, Teng Z (2015) Probiotics inhibit immune fluctuation in the intestinal mucous layer in rats. Surg Today 45:1553–1559

    Article  PubMed  CAS  Google Scholar 

  7. Wu H-J, Wu E (2012) The role of gut microbiota in immune homeostasis and autoimmunity. Gut microbes 3:4–14

    Article  PubMed  PubMed Central  Google Scholar 

  8. Appleton J (2018) The gut-brain axis: influence of microbiota on mood and mental health. Integr Med 17:28

    Google Scholar 

  9. Mohajeri MH, Brummer RJ, Rastall RA, Weersma RK, Harmsen HJ, Faas M, Eggersdorfer M (2018) The role of the microbiome for human health: from basic science to clinical applications. Eur J Nutr 57:1–14

    Article  PubMed  PubMed Central  Google Scholar 

  10. Aragon G, Graham DB, Borum M, Doman DB (2010) Probiotic therapy for irritable bowel syndrome. Gastroenterol Hepatol 6:39

    Google Scholar 

  11. Reiff C, Kelly D (2010) Inflammatory bowel disease, gut bacteria and probiotic therapy. Int J Med Microbiol 300:25–33

    Article  CAS  PubMed  Google Scholar 

  12. Dinan TG, Cryan JF (2017) The microbiome-gut-brain axis in health and disease. Gastroenterol Clin 46:77–89

    Article  Google Scholar 

  13. Bharwani A, Mian MF, Surette MG, Bienenstock J, Forsythe P (2017) Oral treatment with Lactobacillus rhamnosus attenuates behavioural deficits and immune changes in chronic social stress. BMC Med 15:1–14

    Article  CAS  Google Scholar 

  14. Hao Z, Wang W, Guo R, Liu H (2019) Faecalibacterium prausnitzii (ATCC 27766) has preventive and therapeutic effects on chronic unpredictable mild stress-induced depression-like and anxiety-like behavior in rats. Psychoneuroendocrinology 104:132–142

    Article  CAS  PubMed  Google Scholar 

  15. Queiroz JS, Blasco IM, Gagliano H, Daviu N, Román AG, Belda X, Carrasco J, Rocha MC, Neto JP, Armario A (2016) Chlorella vulgaris reduces the impact of stress on hypothalamic–pituitary–adrenal axis and brain c-fos expression. Psychoneuroendocrinology 65:1–8

    Article  CAS  Google Scholar 

  16. Savignac H, Kiely B, Dinan T, Cryan J (2014) B ifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol Motil 26:1615–1627

    Article  CAS  PubMed  Google Scholar 

  17. Ait-Belgnaoui A, Durand H, Cartier C, Chaumaz G, Eutamene H, Ferrier L, Houdeau E, Fioramonti J, Bueno L, Theodorou V (2012) Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37:1885–1895

    Article  CAS  PubMed  Google Scholar 

  18. Giordano R, Pellegrino M, Picu A, Bonelli L, Balbo M, Berardelli R, Lanfranco F, Ghigo E, Arvat E (2006) Neuroregulation of the hypothalamus-pituitary-adrenal (HPA) axis in humans: effects of GABA-, mineralocorticoid-, and GH-Secretagogue-receptor modulation. Sci World J 6:1–11

    Article  CAS  Google Scholar 

  19. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci 108:16050–16055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Aguilar-Toalá J, Garcia-Varela R, Garcia H, Mata-Haro V, González-Córdova A, Vallejo-Cordoba B, Hernández-Mendoza A (2018) Postbiotics: an evolving term within the functional foods field. Trends Food Sci Technol 75:105–114

    Article  CAS  Google Scholar 

  21. Lyte M (2013) Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathog 9:e1003726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Lyte M (2014) Microbial endocrinology and the microbiota-gut-brain axis. In: Lyte Mark, Cryan John F (eds) Microbial endocrinology: the microbiota-gut-brain axis in health and disease. Springer, New York, pp 3–24

    Chapter  Google Scholar 

  23. Boonstra E, de Kleijn R, Colzato LS, Alkemade A, Forstmann BU, Nieuwenhuis S (2015) Neurotransmitters as food supplements: the effects of GABA on brain and behavior. Front Psychol 6:1520

    Article  PubMed  PubMed Central  Google Scholar 

  24. Mazzoli R, Pessione E (2016) The neuro-endocrinological role of microbial glutamate and GABA signaling. Front Microbiol 7:1934

    Article  PubMed  PubMed Central  Google Scholar 

  25. Janik R, Thomason LA, Stanisz AM, Forsythe P, Bienenstock J, Stanisz GJ (2016) Magnetic resonance spectroscopy reveals oral Lactobacillus promotion of increases in brain GABA, N-acetyl aspartate and glutamate. Neuroimage 125:988–995

    Article  CAS  PubMed  Google Scholar 

  26. Yaribeygi H, Panahi Y, Sahraei H, Johnston TP, Sahebkar A (2017) The impact of stress on body function: a review. EXCLI J 16:1057

    PubMed  PubMed Central  Google Scholar 

  27. Joëls M, Karst H, Sarabdjitsingh R (2018) The stressed brain of humans and rodents. Acta Physiol 223:e13066

    Article  CAS  Google Scholar 

  28. Shields GS, Sazma MA, McCullough AM, Yonelinas AP (2017) The effects of acute stress on episodic memory: a meta-analysis and integrative review. Psychol Bull 143:636

    Article  PubMed  PubMed Central  Google Scholar 

  29. Eivani M, Alijanpour S, Arefian E, Rezayof A (2019) Corticolimbic analysis of microRNAs and protein expressions in scopolamine-induced memory loss under stress. Neurobiol Learn Mem 164:107065

    Article  CAS  PubMed  Google Scholar 

  30. Misra S, Medhi B (2013) Role of probiotics as memory enhancer. Indian J Pharmacol 45:311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gareau MG, Wine E, Rodrigues DM, Cho JH, Whary MT, Philpott DJ, MacQueen G, Sherman PM (2011) Bacterial infection causes stress-induced memory dysfunction in mice. Gut 60:307–317

    Article  PubMed  Google Scholar 

  32. Bekinschtein P, Cammarota M, Medina JH (2014) BDNF and memory processing. Neuropharmacology 76:677–683

    Article  CAS  PubMed  Google Scholar 

  33. Gallo FT, Katche C, Morici JF, Medina JH, Weisstaub NV (2018) Immediate early genes, memory and psychiatric disorders: focus on c-Fos, Egr1 and Arc. Front Behav Neurosci 12:79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Katche C, Medina JH (2015) Requirement of an early activation of BDNF/c-Fos cascade in the retrosplenial cortex for the persistence of a long-lasting aversive memory. Cerebral Cortex:bhv284

  35. Leal G, Bramham C, Duarte C (2017) BDNF and hippocampal synaptic plasticity. Vitam Horm 104:153–195

    Article  CAS  PubMed  Google Scholar 

  36. Hendrickx A, Pierrot N, Tasiaux B, Schakman O, Kienlen-Campard P, De Smet C, Octave J-N (2014) Epigenetic regulations of immediate early genes expression involved in memory formation by the amyloid precursor protein of Alzheimer disease. PLoS ONE 9:e99467

    Article  PubMed  PubMed Central  Google Scholar 

  37. Luine V, Frankfurt M (2013) Interactions between estradiol, BDNF and dendritic spines in promoting memory. Neuroscience 239:34–45

    Article  CAS  PubMed  Google Scholar 

  38. Barbosa FF, Santos JR, Meurer YSR, Macêdo PT, Ferreira LMS, Pontes IMO, Ribeiro AM, Silva RH (2013) Differential cortical c-Fos and Zif-268 expression after object and spatial memory processing in a standard or episodic-like object recognition task. Front Behav Neurosci 7:112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Jaworski J, Kalita K, Knapska E (2018) c-Fos and neuronal plasticity: the aftermath of Kaczmarek’s theory. Acta Neurobiol Exp 78:287–296

    Article  Google Scholar 

  40. VanElzakker M, Fevurly RD, Breindel T, Spencer RL (2008) Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex. Learn Mem 15:899–908

    Article  PubMed  PubMed Central  Google Scholar 

  41. Zhang J, Zhang D, McQuade JS, Behbehani M, Tsien JZ, Xu M (2002) C-fos regulates neuronal excitability and survival. Nat Genet 30:416–420

    Article  CAS  PubMed  Google Scholar 

  42. Dong M, Wu Y, Fan Y, Xu M, Zhang J (2006) c-fos modulates brain-derived neurotrophic factor mRNA expression in mouse hippocampal CA3 and dentate gyrus neurons. Neurosci Lett 400:177–180

    Article  CAS  PubMed  Google Scholar 

  43. Spear LP (2013) Adolescent neurodevelopment. J Adolesc Health 52:S7–S13

    Article  PubMed  PubMed Central  Google Scholar 

  44. Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci 108:3047–3052

    Article  CAS  PubMed Central  Google Scholar 

  45. Yahfoufi N, Matar C, Ismail N (2020) Adolescence and aging: Impact of adolescence inflammatory stress and microbiota alterations on brain development, aging, and neurodegeneration. J Gerontol 75:1251–1257

    Article  CAS  Google Scholar 

  46. Codagnone MG, Stanton C, O’Mahony SM, Dinan TG, Cryan JF (2019) Microbiota and neurodevelopmental trajectories: role of maternal and early-life nutrition. Ann Nutr Metab 74:16–27

    Article  CAS  PubMed  Google Scholar 

  47. Heiss CN, Olofsson LE (2019) The role of the gut microbiota in development, function and disorders of the central nervous system and the enteric nervous system. J Neuroendocrinol 31:e12684

    Article  PubMed  CAS  Google Scholar 

  48. Cerdó T, Ruíz A, Suárez A, Campoy C (2017) Probiotic, prebiotic, and brain development. Nutrients 9:1247

    Article  PubMed Central  CAS  Google Scholar 

  49. Abildgaard A, Elfving B, Hokland M, Lund S, Wegener G (2017) Probiotic treatment protects against the pro-depressant-like effect of high-fat diet in Flinders sensitive line rats. Brain Behav Immun 65:33–42

    Article  CAS  PubMed  Google Scholar 

  50. Azagra-Boronat I, Massot-Cladera M, Knipping K, Garssen J, Ben Amor K, Knol J, Franch À, Castell M, Rodríguez-Lagunas MJ, Pérez-Cano FJ (2020) Strain-specific probiotic properties of bifidobacteria and lactobacilli for the prevention of diarrhea caused by rotavirus in a preclinical model. Nutrients 12:498

    Article  CAS  PubMed Central  Google Scholar 

  51. Abildgaard A, Elfving B, Hokland M, Wegener G, Lund S (2017) Probiotic treatment reduces depressive-like behaviour in rats independently of diet. Psychoneuroendocrinology 79:40–48

    Article  CAS  PubMed  Google Scholar 

  52. Barouei J, Moussavi M, Hodgson DM (2012) Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLoS ONE 7:e46051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Fak F, Ahrne S, Molin G, Jeppsson B, Westrom B (2008) Microbial manipulation of the rat dam changes bacterial colonization and alters properties of the gut in her offspring. Am J Physiol Gastrointestinal Liver Physiol 294:G148–G154

    Article  CAS  Google Scholar 

  54. Paxinos G, Watson C (2006) The rat brain in stereotaxic coordinates: hard, cover. Elsevier

    Google Scholar 

  55. Xu L, Holscher C, Anwyl R, Rowan M (1998) Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proc Natl Acad Sci USA 95(6):3204–3208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Rezayof A, Razavi S, Haeri-Rohani A, Rassouli Y, Zarrindast MR (2007) GABAA receptors of hippocampal CA1 regions are involved in the acquisition and expression of morphine-induced place preference. Eur Neuropsychopharmacol 17:24–31

    Article  CAS  PubMed  Google Scholar 

  57. Alijanpour S, Rezayof A, Sepehri H, Delphi L (2015) Alterations in the hippocampal phosphorylated CREB expression in drug state-dependent learning. Behav Brain Res 292:109–115

    Article  CAS  PubMed  Google Scholar 

  58. Taylor SC, Berkelman T, Yadav G, Hammond M (2013) A defined methodology for reliable quantification of Western blot data. Mol Biotechnol 55:217–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Pillai-Kastoori L, Schutz-Geschwender AR, Harford JA (2020) A systematic approach to quantitative Western blot analysis. Anal Biochem 593:113608

    Article  CAS  PubMed  Google Scholar 

  60. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  61. Mahmood T, Yang P-C (2012) Western blot: technique, theory, and trouble shooting. N Am J Med Sci 4:429

    Article  PubMed  PubMed Central  Google Scholar 

  62. Abbasi-Habashi S, Ghasemzadeh Z, Rezayof A (2020) Morphine improved stress-induced amnesia and anxiety through interacting with the ventral hippocampal endocannabinoid system in rats. Brain Res Bull 164:407–414

    Article  CAS  PubMed  Google Scholar 

  63. Musazzi L, Sala N, Tornese P, Gallivanone F, Belloli S, Conte A, Di Grigoli G, Chen F, Ae Ikinci, Treccani G, Bazzini C, Castiglioni I, Nyengaard JR, Wegener G, Moresco RM, Popoli M (2019) Acute inescapable stress rapidly increases synaptic energy metabolism in prefrontal cortex and alters working memory performance. Cerebral Cortex 29:4948–4957

    Article  PubMed  Google Scholar 

  64. Liu Y, Wu Y-W, Qian Z-Q, Yan C-F, Fan K-M, Xu J-H, Li X, Liu Z-Q (2016) Effect of opioid receptors on acute stress-induced changes in recognition memory. Sheng li xue bao: [Acta Physiologica Sinica] 68:757–766

    Google Scholar 

  65. Sardari M, Rezayof A, Khodagholi F (2015) Hippocampal signaling pathways are involved in stress-induced impairment of memory formation in rats. Brain Res 1625:54–63

    Article  CAS  PubMed  Google Scholar 

  66. Chen C-C, Yang C-H, Huang C-C, Hsu K-S (2010) Acute stress impairs hippocampal mossy fiber-CA3 long-term potentiation by enhancing cAMP-specific phosphodiesterase 4 activity. Neuropsychopharmacology 35:1605–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kawakami K, Koga K (2021) Acute elevated platform triggers stress induced hyperalgesia and alters glutamatergic transmission in the adult mice anterior cingulate cortex. IBRO Neuroscience Reports 10:1–7

    Article  PubMed  PubMed Central  Google Scholar 

  68. Ni Y, Yang X, Zheng L, Wang Z, Wu L, Jiang J, Yang T, Ma L, Fu Z (2019) Lactobacillus and Bifidobacterium improves physiological function and cognitive ability in aged mice by the regulation of gut microbiota. Mol Nutr Food Res 63:1900603

    Article  CAS  Google Scholar 

  69. Yang X, Yu D, Xue L, Li H, Du J (2020) Probiotics modulate the microbiota–gut–brain axis and improve memory deficits in aged SAMP8 mice. Acta Pharma Sinica B 10:475–487

    Article  CAS  Google Scholar 

  70. Sarkar SR, Mazumder PM, Banerjee S (2020) Probiotics protect against gut dysbiosis associated decline in learning and memory. J Neuroimmunol 348:577390

    Article  CAS  Google Scholar 

  71. Romo-Araiza A, Gutiérrez-Salmeán G, Galván EJ, Hernández-Frausto M, Herrera-López G, Romo-Parra H, García-Contreras V, Fernández-Presas AM, Jasso-Chávez R, Borlongan CV (2018) Probiotics and prebiotics as a therapeutic strategy to improve memory in a model of middle-aged rats. Front Aging Neurosci 10:416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ait-Belgnaoui A, Colom A, Braniste V, Ramalho L, Marrot A, Cartier C, Houdeau E, Theodorou V, Tompkins T (2014) Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroenterol Motil 26:510–520

    Article  CAS  PubMed  Google Scholar 

  73. Xiao J, Wang T, Xu Y, Gu X, Li D, Niu K, Wang T, Zhao J, Zhou R, Wang H-L (2020) Long-term probiotic intervention mitigates memory dysfunction through a novel H3K27me3-based mechanism in lead-exposed rats. Transl Psych 10:1–18

    CAS  Google Scholar 

  74. Markowiak P, Śliżewska K (2017) Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9:1021

    Article  PubMed Central  CAS  Google Scholar 

  75. Markowiak P, Śliżewska K (2018) The role of probiotics, prebiotics and synbiotics in animal nutrition. Gut pathogens 10:1–20

    Article  CAS  Google Scholar 

  76. Kim JJ, Koo JW, Lee HJ, Han J-S (2005) Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J Neurosci 25:1532–1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Yoto A, Murao S, Motoki M, Yokoyama Y, Horie N, Takeshima K, Masuda K, Kim M, Yokogoshi H (2012) Oral intake of γ-aminobutyric acid affects mood and activities of central nervous system during stressed condition induced by mental tasks. Amino Acids 43:1331–1337

    Article  CAS  PubMed  Google Scholar 

  78. Diez-Gutiérrez L, San Vicente L, Barron LJR, del Carmen VM, Chávarri M (2020) Gamma-aminobutyric acid and probiotics: multiple health benefits and their future in the global functional food and nutraceuticals market. J Funct Foods 64:103669

    Article  CAS  Google Scholar 

  79. Barrett E, Ross R, O’Toole PW, Fitzgerald GF, Stanton C (2012) γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 113:411–417

    Article  CAS  PubMed  Google Scholar 

  80. Cui Y, Miao K, Niyaphorn S, Qu X (2020) Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. Int J Mol Sci 21:995

    Article  CAS  PubMed Central  Google Scholar 

  81. Yunes RA, Poluektova EU, Dyachkova MS, Klimina KM, Kovtun AS, Averina OV, Orlova VS, Danilenko VN (2016) GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strains from human microbiota. Anaerobe 42:197–204

    Article  CAS  PubMed  Google Scholar 

  82. Boonstra E, de Kleijn R, Colzato LS, Alkemade A, Forstmann BU, Nieuwenhuis S (2015) Neurotransmitters as food supplements: the effects of GABA on brain and behavior. Front Psychol. https://doi.org/10.3389/fpsyg.2015.01520

    Article  PubMed  PubMed Central  Google Scholar 

  83. Bermúdez-Humarán LG, Salinas E, Ortiz GG, Ramirez-Jirano LJ, Morales JA, Bitzer-Quintero OK (2019) From probiotics to psychobiotics: live beneficial bacteria which act on the brain-gut axis. Nutrients 11:890

    Article  PubMed Central  CAS  Google Scholar 

  84. Liang L, Zhou H, Zhang S, Yuan J, Wu H (2017) Effects of gut microbiota disturbance induced in early life on the expression of extrasynaptic GABA-A receptor#±5 and#´ subunits in the hippocampus of adult rats. Brain Res Bull 135:113–119

    Article  CAS  PubMed  Google Scholar 

  85. Tabouy L, Getselter D, Ziv O, Karpuj MV, Te T, Lukic I, Maayouf R, Werbner N, Ben-Amram H, Nuriel-Ohayon M, Koren O, Elliott E (2018) Dysbiosis of microbiome and probiotic treatment in a genetic model of autism spectrum disorders. Brain Behav Immun 73:310–319

    Article  PubMed  Google Scholar 

  86. Liu Y-W, Liu W-H, Wu C-C, Juan Y-C, Wu Y-c, Tsai H-P, Wang S, Tsai Y-C (2016) Psychotropic effects of Lactobacillus plantarum PS128 in early life-stressed and naïve adult mice. Brain Res 1631:1–12

    Article  CAS  PubMed  Google Scholar 

  87. Jeong J-J, Kim K-A, Ahn YT, Sim J, Woo J-Y, Huh CS, Kim D-H (2015) Probiotic mixture KF attenuates age-dependent memory deficit and lipidemia in Fischer 344 Rats. J Microbiol Biotechnol 25(9):1532–1536

    Article  CAS  PubMed  Google Scholar 

  88. Wang H, Lee I-s, Braun C, Enck P (2016) Effect of probiotics on central nervous system functions in animals and humans: a systematic review. J Neurogastroenterol Motility 22:589–605

    Article  CAS  Google Scholar 

  89. Wu C-H, Hsueh Y-H, Kuo JM, Liu S (2018) Characterization of a Potential Probiotic Lactobacillus brevis RK03 and Efficient Production of#3-Aminobutyric Acid in Batch Fermentation. Int J Mol Sci 19

  90. Ishikawa R, Fukushima H, Nakakita Y, Kado H, Kida S (2019) Dietary heat-killed Lactobacillus brevis SBC 8803 (SBL 88™) improves hippocampus-dependent memory performance and adult hippocampal neurogenesis. Neuropsychopharmacol Rep 39:140–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Jeong J-J, Kim KA, Hwang YJ, Han MJ, Kim D-H (2016) Anti-inflammaging effects of Lactobacillus brevis OW38 in aged mice. Beneficial Microbes 7(5):707–718

    Article  CAS  PubMed  Google Scholar 

  92. Steenbergen L, Sellaro R, Sv H, Bosch JA, Colzato LS (2015) A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav Immun 48:258–264

    Article  PubMed  Google Scholar 

  93. Culpepper T, Christman MC, Nieves C, Specht GJ, Rowe CC, Spaiser SJ, Ford AL, Dahl WJ, Girard SA, Langkamp-Henken B (2016) Bifidobacterium bifidum R0071 decreases stress-associated diarrhoea-related symptoms and self-reported stress: a secondary analysis of a randomised trial. Beneficial microbes 7(3):327–336

    Article  CAS  PubMed  Google Scholar 

  94. Yang X, Yu D, Xue L, Li H, Du J (2020) Probiotics modulate the microbiot gut brain axis and improve memory deficits in aged SAMP8 mice. Acta Pharma Sinica B 10:475–487

    Article  CAS  Google Scholar 

  95. Haghighat N, Rajabi S, Mohammadshahi M (2019) Effect of synbiotic and probiotic supplementation on serum brain-derived neurotrophic factor level, depression and anxiety symptoms in hemodialysis patients: a randomized, double-blinded, clinical trial. Nutr Neurosci 24:490–499

    Article  PubMed  Google Scholar 

  96. Scriven M, Dinan TG, Cryan JF, Wall M (2018) Neuropsychiatric Disorders: Influence of Gut Microbe to Brain Signalling. Diseases 6

  97. Katche C, Bekinschtein P, Slipczuk L, Goldin A, Izquierdo I, Cammarota M, Medina JH (2009) Delayed wave of c-Fos expression in the dorsal hippocampus involved specifically in persistence of long-term memory storage. Proc Natl Acad Sci 107:349–354

    Article  PubMed  PubMed Central  Google Scholar 

  98. Liang S, Wang T, Hu X, Luo J, Li W, Wu X, Duan Y, Jin F (2015) Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience 310:561–577

    Article  CAS  PubMed  Google Scholar 

  99. Rocher C, Spedding M, Muñoz C, Jay TM (2004) Acute stress-induced changes in hippocampal/prefrontal circuits in rats: effects of antidepressants. Cereb Cortex 14(2):224–229

    Article  PubMed  Google Scholar 

  100. Zoladz PR, Park CR, Halonen JD, Salim S, Alzoubi KH, Srivareerat M, Fleshner M, Alkadhi KA, Diamond DM (2012) Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress induced amnesia. Hippocampus 22:577–589

    Article  CAS  PubMed  Google Scholar 

  101. Adlard PA, Cotman C (2004) Voluntary exercise protects against stress-induced decreases in brain-derived neurotrophic factor protein expression. Neuroscience 124:985–992

    Article  CAS  PubMed  Google Scholar 

  102. Xu H, Chen Z, He J, Haimanot S, Li X, Dyck LE, Li X-M (2006) Synergetic effects of quetiapine and venlafaxine in preventing the chronic restraint stress induced decrease in cell proliferation and BDNF expression in rat hippocampus. Hippocampus 16

  103. Liu J, Sun J, Wang F, Yu X, Ling Z, Li H, Zhang H, Jin J, Chen W, Pang M, Yu J, He Y, Xu J (2015) Neuroprotective effects of clostridium butyricum against vascular dementia in mice via metabolic butyrate. BioMed Res Int 2015

  104. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu X-N, Kubo C, Koga Y (2004) Postnatal microbial colonization programs the hypothalamiƒ pituitary adrenal system for stress response in mice. J Physiol 558

  105. Jena A, Montoya CA, Mullaney JA, Dilger RN, Young W, McNabb WC, Roy NC (2020) Gut-brain axis in the early postnatal years of life: a developmental perspective. Frontiers in Integrative Neuroscience. https://doi.org/10.3389/fnint.2020.00044

    Article  PubMed  PubMed Central  Google Scholar 

  106. Vilar M, Mira H (2016) Regulation of neurogenesis by neurotrophins during adulthood: expected and unexpected roles. Front Neurosci. https://doi.org/10.3389/fnins.2016.0002

    Article  PubMed  PubMed Central  Google Scholar 

  107. Fleischmann A, Hvalby O, Jensen VR, Strekalova T, Zacher CK, Layer LE, Kvello A, Reschke M, Spanagel R, Sprengel R, Wagner EF, Gass P (2003) Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 23:9116–9122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Kaur H, Golovko SA, Golovko MY, Singh S, Darland DC, Combs C (2020) Effects of probiotic supplementation on short chain fatty acids in the appnl-g-f mouse model of Alzheimer’s disease. J Alzheimer’s Dis: JAD 76:1083–1102

    Article  CAS  PubMed  Google Scholar 

  109. Tomás FJB, Turko P, Heilmann H, Trimbuch T, Yanagawa Y, Vida I, Münster-Wandowski A (2020) BDNF expression in cortical GABAergic interneurons. Int J Mol Sci 21:1567

    Article  PubMed Central  CAS  Google Scholar 

  110. Staiger J, Masanneck C, Bisler S, Schleicher A, Zuschratter W, Zilles K (2002) Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment. Neuroscience 109:687–699

    Article  CAS  PubMed  Google Scholar 

  111. Porcher C, Medina I, Gaiarsa J-L (2018) Mechanism of BDNF modulation in GABAergic synaptic transmission in healthy and disease brains. Front Cell Neurosci 12:273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Department of Animal Biology, School of Biology, College of Science, University of Tehran, P. O. Box, Tehran, 4155-6455, Iran

    Kimia Alizadeh, Ali Golbabaei & Ameneh Rezayof

  2. Department of Microbial Biotechnology, School of Biology, College of Science, University of Tehran, Tehran, Iran

    Hamid Moghimi

  3. Department of Biology, Faculty of Science, Gonbad Kavous University, Gonbad Kavous, Iran

    Sakineh Alijanpour

Authors
  1. Kimia Alizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hamid Moghimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ali Golbabaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sakineh Alijanpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ameneh Rezayof
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by all authors. The first draft of the manuscript was written by Ameneh Rezayof, Sakineh Alijanpour and Kimia Alizadeh. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Ameneh Rezayof.

Ethics declarations

Conflict of Interests

The authors declare no conflict of interest, financial or otherwise.

Ethical Approval

All animal treatment procedures were performed by the standard ethical guidelines (NIH, publication no. 85–23, revised 1985; European Communities Directive 86/609/EEC) and were approved by the local ethical committee. All efforts were made to minimize the number of animals used and their suffering.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alizadeh, K., Moghimi, H., Golbabaei, A. et al. Post-Weaning Treatment with Probiotic Inhibited Stress-Induced Amnesia in Adulthood Rats: The Mediation of GABAergic System and BDNF/c-Fos Signaling Pathways. Neurochem Res 47, 2357–2372 (2022). https://doi.org/10.1007/s11064-022-03625-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-022-03625-w

Keywords

Search

Navigation