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The role of the gut microbiota and nutrition on spatial learning and spatial memory: a mini review based on animal studies

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Abstract

The gut-brain axis is believed to constitute a bidirectional communication mechanism that affects both mental and digestive processes. Recently, the role of the gut microbiota in cognitive performance has been the focus of much research. In this paper, we discuss the effects of gut microbiota and nutrition on spatial memory and learning. Studies have shown the influence of diet on cognitive capabilities such as spatial learning and memory. It has been reported that a high-fat diet can alter gut microbiota which subsequently leads to changes in spatial learning and memory. Some microorganisms in the gut that can significantly affect spatial learning and memory are Akkermansia muciniphila, Bifidobacterium, Lactobacillus, Firmicutes, Bacteroidetes, and Helicobacter pylori. For example, a reduction in the amount of A. muciniphila in the gut leads to increased intestinal permeability and induces immune response in the brain which then negatively affects cognitive performances. We suggest that more studies should be carried out regarding the indirect effects of nutrition on cognitive activities via alteration in gut microbiota.

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References

  1. Sender R, Fuchs S, Milo R (2016) Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:337–340

    Article  CAS  PubMed  Google Scholar 

  2. Qin J, Li R, Raes J et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Fung TC, Olson CA, Hsiao EY (2017) Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 20:145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ascher S, Reinhardt C (2018) The gut microbiota: an emerging risk factor for cardiovascular and cerebrovascular disease. Eur J Immunol 48:564–575

    Article  CAS  PubMed  Google Scholar 

  5. Sampson TR, Mazmanian SK (2015) Control of brain development, function, and behavior by the microbiome. Cell Host Microb 17:565–576

    Article  CAS  Google Scholar 

  6. Virtue AT, McCright SJ, Wright JM et al (2019) The gut microbiota regulates white adipose tissue inflammation and obesity via a family of microRNAs. Sci Transl Med 11:eaav1892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Sikalidis AK, Maykish A (2020) The gut microbiome and type 2 diabetes mellitus: discussing a complex relationship. Biomedicines 8:8

    Article  CAS  PubMed Central  Google Scholar 

  8. Dinan TG, Cryan JF, Stanton C (2018) Gut microbes and brain development have black box connectivity. Biol Psychiatry 83:97–99

    Article  PubMed  Google Scholar 

  9. Harach T, Marungruang N, Duthilleul N et al (2017) Reduction of Abeta amyloid pathology in APPPS1 transgenic mice in the absence of gut microbiota. Sci Rep 7:41802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cheke LG, Simons JS, Clayton NS (2016) Higher body mass index is associated with episodic memory deficits in young adults. Q J Exp Psychol 69:2305–2316

    Article  Google Scholar 

  11. Kanoski SE, Davidson TL (2011) Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiol Behav 103:59–68

    Article  CAS  PubMed  Google Scholar 

  12. Alzoubi KH, Mayyas FA, Mahafzah R, Khabour OF (2018) Melatonin prevents memory impairment induced by high-fat diet: role of oxidative stress. Behav Brain Res 336:93–98

    Article  CAS  PubMed  Google Scholar 

  13. Tan BL, Norhaizan ME (2019) Effect of high-fat diets on oxidative stress, cellular inflammatory response and cognitive function. Nutrition 11:2579

    CAS  Google Scholar 

  14. Travica N, D’Cunha NM, Naumovski N et al (2020) The effect of blueberry interventions on cognitive performance and mood: a systematic review of randomized controlled trials. Brain Behav Immunity 85:96–105

    Article  CAS  Google Scholar 

  15. Kendig MD, Boakes RA, Rooney KB, Corbit LH (2013) Chronic restricted access to 10% sucrose solution in adolescent and young adult rats impairs spatial memory and alters sensitivity to outcome devaluation. Physiol Behav 120:164–172

    Article  CAS  PubMed  Google Scholar 

  16. Ebenezer PJ, Wilson CB, Wilson LD, Nair AR (2016) The anti-inflammatory effects of blueberries in an animal model of post-traumatic stress disorder (PTSD). PLoS ONE 11:e0160923

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Travica N, D’Cunha NM, Naumovski N et al (2019) The effect of blueberry interventions on cognitive performance and mood: a systematic review of randomized controlled trials. Brain Behav Immunity 85:96

    Article  CAS  Google Scholar 

  18. Kalaria RN (2012) Cerebrovascular disease and mechanisms of cognitive impairment: evidence from clinicopathological studies in humans. Stroke 43:2526–2534

    Article  PubMed  Google Scholar 

  19. Kaptan Z, Akgün-Dar K, Kapucu A, Dedeakayoğulları H, Batu Ş, Üzüm G (2015) Long term consequences on spatial learning-memory of low-calorie diet during adolescence in female rats; hippocampal and prefrontal cortex BDNF level, expression of NeuN and cell proliferation in dentate gyrus. Brain Res 1618:194–204

    Article  CAS  PubMed  Google Scholar 

  20. Linnarsson S, Willson CA, Ernfors P (2000) Cell death in regenerating populations of neurons in BDNF mutant mice. Mol Brain Res 75:61–69

    Article  CAS  PubMed  Google Scholar 

  21. Gomez-Pinilla F (2008) The influences of diet and exercise on mental health through hormesis. Ageing Res Rev 7:49–62

    Article  CAS  PubMed  Google Scholar 

  22. Stakos DA, Stamatelopoulos K, Bampatsias D et al (2020) The Alzheimer’s disease amyloid-beta hypothesis in cardiovascular aging and disease: JACC focus seminar. J Am Coll Cardiol 75:952–967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hardy JA, Higgins GA (1992) Alzheimer’s disease: the amyloid cascade hypothesis. Science 256:184–186

    Article  CAS  PubMed  Google Scholar 

  24. Ehrlich D, Humpel C (2012) Chronic vascular risk factors (cholesterol, homocysteine, ethanol) impair spatial memory, decline cholinergic neurons and induce blood–brain barrier leakage in rats in vivo. J Neurol Sci 322:92–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sharma S, Rakoczy S, Brown-Borg H (2010) Assessment of spatial memory in mice. Life Sci 87:521–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhang P, Yu Y, Qin Y et al (2019) Alterations to the microbiota–colon–brain axis in high-fat-diet-induced obese mice compared to diet-resistant mice. J Nutr Biochem 65:54–65

    Article  CAS  PubMed  Google Scholar 

  27. Yu Y, Cai Z, Zheng J et al (2012) Serum levels of polyunsaturated fatty acids are low in Chinese men with metabolic syndrome, whereas serum levels of saturated fatty acids, zinc, and magnesium are high. Nutr Res 32:71–77

    Article  CAS  PubMed  Google Scholar 

  28. Miles KN, Skelton MR (2020) Male mice placed on a ketogenic diet from postnatal day (P) 21 through adulthood have reduced growth, are hypoactive, show increased freezing in a conditioned fear paradigm, and have spatial learning deficits. Brain Res 1734:146697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. McLean FH, Grant C, Morris AC et al (2018) Rapid and reversible impairment of episodic memory by a high-fat diet in mice. Sci Rep 8:1–9

    Article  CAS  Google Scholar 

  30. Boitard C, Cavaroc A, Sauvant J et al (2014) Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain Behav Immunity 40:9–17

    Article  CAS  Google Scholar 

  31. Yang Y, Zhong Z, Wang B et al (2019) Early-life high-fat diet-induced obesity programs hippocampal development and cognitive functions via regulation of gut commensal Akkermansia muciniphila. Neuropsychopharmacology 44:2054–2064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Higarza SG, Arboleya S, Gueimonde M, Gómez-Lázaro E, Arias JL, Arias N (2019) Neurobehavioral dysfunction in non-alcoholic steatohepatitis is associated with hyperammonemia, gut dysbiosis, and metabolic and functional brain regional deficits. PLoS ONE 14:e0223019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Deshpande NG, Saxena J, Pesaresi TG et al (2019) High fat diet alters gut microbiota but not spatial working memory in early middle-aged Sprague Dawley rats. PLoS ONE 14:e0217553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Xiao S, Zhang Z, Chen M et al (2019) Xiexin Tang ameliorates dyslipidemia in high-fat diet-induced obese rats via elevating gut microbiota-derived short chain fatty acids production and adjusting energy metabolism. J Ethnopharmacol 241:112032

    Article  PubMed  Google Scholar 

  35. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai L-H (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447:178–182

    Article  CAS  PubMed  Google Scholar 

  36. Govindarajan N, Agis-Balboa RC, Walter J, Sananbenesi F, Fischer A (2011) Sodium butyrate improves memory function in an Alzheimer’s disease mouse model when administered at an advanced stage of disease progression. J Alzheimer’s Dis 26:187–197

    Article  CAS  Google Scholar 

  37. Stilling RM, van de Wouw M, Clarke G, Stanton C, Dinan TG, Cryan JF (2016) The neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis? Neurochem Int 99:110–132

    Article  CAS  PubMed  Google Scholar 

  38. Levenson JM, O’Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD (2004) Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279:40545–40559

    Article  CAS  PubMed  Google Scholar 

  39. Topuz RD, Gunduz O, Tastekin E, Karadag CH (2019) Effects of hippocampal histone acetylation and HDAC inhibition on spatial learning and memory in the Morris water maze in rats. Fundam Clin Pharmacol 34:222

    Article  PubMed  CAS  Google Scholar 

  40. Bilbo SD, Tsang V (2010) Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J 24:2104–2115

    Article  CAS  PubMed  Google Scholar 

  41. White CL, Pistell PJ, Purpera MN et al (2009) Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiol Dis 35:3–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Tozuka Y, Kumon M, Wada E, Onodera M, Mochizuki H, Wada K (2010) Maternal obesity impairs hippocampal BDNF production and spatial learning performance in young mouse offspring. Neurochem Int 57:235–247

    Article  CAS  PubMed  Google Scholar 

  43. de la Monte SM, Longato L, Tong M, Wands JR (2009) Insulin resistance and neurodegeneration: roles of obesity, type 2 diabetes mellitus and non-alcoholic steatohepatitis. Curr Opin Investig Drugs (London, England: 2000) 10:1049

    Google Scholar 

  44. Wong A, Dogra VR, Reichelt AC (2017) High-sucrose diets in male rats disrupt aspects of decision making tasks, motivation and spatial memory, but not impulsivity measured by operant delay-discounting. Behav Brain Res 327:144–154

    Article  CAS  PubMed  Google Scholar 

  45. Buyukata C, Vukalo M, Xu TJ, Khore MA, Reichelt AC (2018) Impact of high sucrose diets on the discrimination of spatial and object memories with overlapping features. Physiol Behav 192:127–133

    Article  CAS  PubMed  Google Scholar 

  46. Abbott KN, Morris MJ, Westbrook RF, Reichelt AC (2016) Sex-specific effects of daily exposure to sucrose on spatial memory performance in male and female rats, and implications for estrous cycle stage. Physiol Behav 162:52–60

    Article  CAS  PubMed  Google Scholar 

  47. Leigh S-J, Kaakoush NO, Bertoldo MJ, Westbrook RF, Morris MJ (2020) Intermittent cafeteria diet identifies fecal microbiome changes as a predictor of spatial recognition memory impairment in female rats. Physiol Behav 10:1–12

    Google Scholar 

  48. He A, Zhang Y, Yang Y et al (2017) Prenatal high sucrose intake affected learning and memory of aged rat offspring with abnormal oxidative stress and NMDARs/Wnt signaling in the hippocampus. Brain Res 1669:114–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Sen T, Cawthon CR, Ihde BT et al (2017) Diet-driven microbiota dysbiosis is associated with vagal remodeling and obesity. Physiol Behav 173:305–317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Noble EE, Hsu TM, Kanoski SE (2017) Gut to brain dysbiosis: mechanisms linking western diet consumption, the microbiome, and cognitive impairment. Front Behav Neurosci 11:9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Cordain L, Eaton SB, Sebastian A et al (2005) Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 81:341–354

    Article  CAS  PubMed  Google Scholar 

  52. Christ A, Lauterbach M, Latz E (2019) Western diet and the immune system: an inflammatory connection. Immun 51:794–811

    Article  CAS  Google Scholar 

  53. Patterson E, O’Doherty RM, Murphy EF et al (2014) Impact of dietary fatty acids on metabolic activity and host intestinal microbiota composition in C57BL/6J mice. Br J Nutr 111:1905–1917

    Article  CAS  PubMed  Google Scholar 

  54. Daulatzai MA (2014) Obesity and gut’s dysbiosis promote neuroinflammation, cognitive impairment, and vulnerability to Alzheimer’s disease: new directions and therapeutic implications. J Mol Genet Med S 1:05

    Google Scholar 

  55. Ohland CL, Kish L, Bell H et al (2013) Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology 38:1738–1747

    Article  CAS  PubMed  Google Scholar 

  56. Magnusson K, Hauck L, Jeffrey B et al (2015) Relationships between diet-related changes in the gut microbiome and cognitive flexibility. Neuroscience 300:128–140

    Article  CAS  PubMed  Google Scholar 

  57. Kosari S, Badoer E, Nguyen JC, Killcross AS, Jenkins TA (2012) Effect of western and high fat diets on memory and cholinergic measures in the rat. Behav Brain Res 235:98–103

    Article  CAS  PubMed  Google Scholar 

  58. Val-Laillet D, Besson M, Guérin S et al (2017) A maternal Western diet during gestation and lactation modifies offspring’s microbiota activity, blood lipid levels, cognitive responses, and hippocampal neurogenesis in Yucatan pigs. FASEB J 31:2037–2049

    Article  CAS  PubMed  Google Scholar 

  59. Hwang IK, Kim IY, Kim YN et al (2009) Comparative study on high fat diet-induced 4-hydroxy-2E-nonenal adducts in the hippocampal CA1 region of C57BL/6N and C3H/HeN mice. Neurochem Res 34:964–972

    Article  CAS  PubMed  Google Scholar 

  60. Rajilić-Stojanović M, de Vos WM (2014) The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev 38:996–1047

    Article  PubMed  CAS  Google Scholar 

  61. Brahe LK, Le Chatelier E, Prifti E et al (2015) Specific gut microbiota features and metabolic markers in postmenopausal women with obesity. Nutr Diabetes 5:e159–e159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ou Z, Deng L, Lu Z et al (2020) Protective effects of Akkermansia muciniphila on cognitive deficits and amyloid pathology in a mouse model of Alzheimer’s disease. Nutr Diab 10:1–10

    Article  CAS  Google Scholar 

  63. Wu F, Guo X, Zhang M et al (2020) An Akkermansia muciniphila subtype alleviates high-fat diet-induced metabolic disorders and inhibits the neurodegenerative process in mice. Anaerobe 61:102138

    Article  CAS  PubMed  Google Scholar 

  64. Grander C, Adolph TE, Wieser V et al (2018) Recovery of ethanol-induced Akkermansia muciniphila depletion ameliorates alcoholic liver disease. Gut 67:891–901

    Article  PubMed  CAS  Google Scholar 

  65. Pistollato F, Sumalla Cano S, Elio I, Masias Vergara M, Giampieri F, Battino M (2016) Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr Rev 74:624–634

    Article  PubMed  Google Scholar 

  66. Hill JM, Lukiw WJ (2015) Microbial-generated amyloids and Alzheimer’s disease (AD). Front Aging Neurosci 7:9

    Article  PubMed  PubMed Central  Google Scholar 

  67. Wong CB, Odamaki T, Xiao J-z (2019) Beneficial effects of Bifidobacterium longum subsp. longum BB536 on human health: Modulation of gut microbiome as the principal action. J Funct Foods 54:506–519

    Article  CAS  Google Scholar 

  68. Iwabuchi N, Hiruta N, Shimizu K, Yaeshima T, Iwatsuki K, Yasui H (2009) Effects of intranasal administration of Bifidobacterium longum BB536 on mucosal immune system in respiratory tract and influenza virus infection in mice. Milk Sci 58:129–133

    CAS  Google Scholar 

  69. Del Giudice MM, Indolfi C, Capasso M, Maiello N, Decimo F, Ciprandi G (2017) Bifidobacterium mixture (B longum BB536, B infantis M-63, B breve M-16V) treatment in children with seasonal allergic rhinitis and intermittent asthma. Ital J Pediatr 43:25

    Article  PubMed Central  CAS  Google Scholar 

  70. Yeşilyurt N, Yılmaz B, Ağagündüz D, Capasso R (2021) Involvement of probiotics and postbiotics in the immune system modulation. Biologics 1:89–110

    Article  Google Scholar 

  71. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG (2010) Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neurosci 170:1179–1188

    Article  CAS  Google Scholar 

  72. Davari S, Talaei SA, Alaei H (2013) Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome–gut–brain axis. Neurosci 240:287–296

    Article  CAS  Google Scholar 

  73. O’Hagan C, Li JV, Marchesi JR, Plummer S, Garaiova I, Good MA (2017) Long-term multi-species Lactobacillus and Bifidobacterium dietary supplement enhances memory and changes regional brain metabolites in middle-aged rats. Neurobiol Learn Mem 144:36–47

    Article  CAS  PubMed  Google Scholar 

  74. Asl ZR, Sepehri G, Salami M (2019) Probiotic treatment improves the impaired spatial cognitive performance and restores synaptic plasticity in an animal model of Alzheimer’s disease. Behav Brain Res 376:112183

    Article  CAS  Google Scholar 

  75. Rezaeiasl Z, Salami M, Sepehri G (2019) The effects of probiotic lactobacillus and bifidobacterium strains on memory and learning behavior, long-term potentiation (LTP), and some biochemical parameters in β-amyloid-induced rat’s model of Alzheimer’s disease. Prev Nutr Food Sci 24:265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bagheri S, Heydari A, Alinaghipour A, Salami M (2019) Effect of probiotic supplementation on seizure activity and cognitive performance in PTZ-induced chemical kindling. Epilepsy Behav 95:43–50

    Article  PubMed  Google Scholar 

  77. Tahmasebi S, Oryan S, Mohajerani HR, Akbari N, Palizvan MR (2020) Probiotics and Nigella sativa extract supplementation improved behavioral and electrophysiological effects of PTZ-induced chemical kindling in rats. Epilepsy Behav 104:106897

    Article  PubMed  Google Scholar 

  78. Athari Nik Azm S, Djazayeri A, Safa M et al (2018) Lactobacilli and bifidobacteria ameliorate memory and learning deficits and oxidative stress in β-amyloid (1–42) injected rats. Appl Physiol Nutr Metab 43:718–726

    Article  CAS  PubMed  Google Scholar 

  79. de Cossío LF, Fourrier C, Sauvant J et al (2017) Impact of prebiotics on metabolic and behavioral alterations in a mouse model of metabolic syndrome. Brain Behav Immunity 64:33–49

    Article  CAS  Google Scholar 

  80. Rahmati H, Momenabadi S, Vafaei AA, Bandegi AR, Mazaheri Z, Vakili A (2019) Probiotic supplementation attenuates hippocampus injury and spatial learning and memory impairments in a cerebral hypoperfusion mouse model. Mol Biol Rep 46:4985–4995

    Article  CAS  PubMed  Google Scholar 

  81. Lye H-S, Kuan C-Y, Ewe J-A, Fung W-Y, Liong M-T (2009) The improvement of hypertension by probiotics: effects on cholesterol, diabetes, renin, and phytoestrogens. Int J Mol Sci 10:3755–3775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Jeong JJ, Woo JY, Kim KA, Han M, Kim DH (2015) Lactobacillus pentosus var. plantarum C29 ameliorates age-dependent memory impairment in F ischer 344 rats. Lett Appl Microbiol 60:307–314

    Article  CAS  PubMed  Google Scholar 

  83. Mariat D, Firmesse O, Levenez F et al (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9:123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Crovesy L, Masterson D, Rosado EL (2020) Profile of the gut microbiota of adults with obesity: a systematic review. Eur J Clin Nutr 74:1–12

    Article  Google Scholar 

  85. Zhao L, Lou H, Peng Y, Chen S, Zhang Y, Li X (2019) Comprehensive relationships between gut microbiome and faecal metabolome in individuals with type 2 diabetes and its complications. Endocrine 66:526–537

    Article  CAS  PubMed  Google Scholar 

  86. Kinross JM, Darzi AW, Nicholson JK (2011) Gut microbiome-host interactions in health and disease. Genome Med 3:14

    Article  PubMed  PubMed Central  Google Scholar 

  87. Shimizu C, Wakita Y, Kihara M, Kobayashi N, Tsuchiya Y, Nabeshima T (2019) Association of lifelong intake of barley diet with healthy aging: Changes in physical and cognitive functions and intestinal microbiome in senescence-accelerated mouse-prone 8 (samp8). Nutrition 11:1770

    CAS  Google Scholar 

  88. Xiao Y, Dong J, Yin Z, Wu Q, Zhou Y, Zhou X (2018) Procyanidin B2 protects against d-galactose-induced mimetic aging in mice: metabolites and microbiome analysis. Food Chem Toxicol 119:141–149

    Article  CAS  PubMed  Google Scholar 

  89. Bercik P, Denou E, Collins J et al (2011) The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141:599–609

    Article  CAS  PubMed  Google Scholar 

  90. Karakan T, Ozkul C, Küpeli Akkol E, Bilici S, Sobarzo-Sánchez E, Capasso R (2021) Gut-brain-microbiota axis: antibiotics and functional gastrointestinal disorders. Nutrition 13:389

    CAS  Google Scholar 

  91. Guida F, Turco F, Iannotta M et al (2018) Antibiotic-induced microbiota perturbation causes gut endocannabinoidome changes, hippocampal neuroglial reorganization and depression in mice. Brain Behav Immunol 67:230–245

    Article  CAS  Google Scholar 

  92. Zhang C, Zhang M, Pang X, Zhao Y, Wang L, Zhao L (2012) Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. ISME J 6:1848–1857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kong C, Gao R, Yan X, Huang L, Qin H (2019) Probiotics improve gut microbiota dysbiosis in obese mice fed a high-fat or high-sucrose diet. Nutrition 60:175–184

    Article  CAS  PubMed  Google Scholar 

  94. Testerman TL, Morris J (2014) Beyond the stomach: an updated view of Helicobacter pylori pathogenesis, diagnosis, and treatment. World J Gastroenterol: WJG 20:12781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Öztekin M, Yılmaz B, Ağagündüz D, Capasso R (2021) Overview of Helicobacter pylori Infection: clinical features, treatment, and nutritional aspects. Disease 9:66

    Article  CAS  Google Scholar 

  96. Arzani M, Jahromi SR, Ghorbani Z et al (2020) Gut-brain Axis and migraine headache: a comprehensive review. J Headache Pain 21:1–12

    Article  Google Scholar 

  97. McGee DJ, Lu X-H, Disbrow EA (2018) Stomaching the possibility of a pathogenic role for Helicobacter pylori in Parkinson’s disease. J Parkinson’s Dis 8:367–374

    Article  Google Scholar 

  98. Wang X-L, Zeng J, Feng J et al (2014) Helicobacter pylori filtrate impairs spatial learning and memory in rats and increases β-amyloid by enhancing expression of presenilin-2. Front Aging Neurosci 6:66

    Article  PubMed  PubMed Central  Google Scholar 

  99. Shen L, Liu L, Ji H-F (2017) Alzheimer’s disease histological and behavioral manifestations in transgenic mice correlate with specific gut microbiome state. J Alzheimer’s Dis 56:385–390

    Article  CAS  Google Scholar 

  100. Reichelt AC, Killcross S, Hambly LD, Morris MJ, Westbrook RF (2015) Impact of adolescent sucrose access on cognitive control, recognition memory, and parvalbumin immunoreactivity. Learn Mem 22:215–224

    Article  PubMed  PubMed Central  Google Scholar 

  101. Reichelt AC, Morris MJ, Westbrook RF (2016) Daily access to sucrose impairs aspects of spatial memory tasks reliant on pattern separation and neural proliferation in rats. Learn Mem 23:386–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Alemohammad, S.M.A., Noori, S.M.R., Samarbafzadeh, E. et al. The role of the gut microbiota and nutrition on spatial learning and spatial memory: a mini review based on animal studies. Mol Biol Rep 49, 1551–1563 (2022). https://doi.org/10.1007/s11033-021-07078-2

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