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CNS & Neurological Disorders - Drug Targets

Author(s): Joyal Xavier, M. Anu, A.S. Fathima, V. Ravichandiran and Nitesh Kumar*

DOI: 10.2174/1871527321666220614124145

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Intriguing Role of Gut-Brain Axis on Cognition with an Emphasis on Interaction with Papez Circuit

Page: [1146 - 1163] Pages: 18

  • * (Excluding Mailing and Handling)

Abstract

The gut microbiome is a complicated ecosystem of around a hundred billion symbiotic bacteria cells. Bidirectional communication between the gut and the brain is facilitated by the immune system, the enteric nervous system, the vagus nerve, and microbial compounds such as tryptophan metabolites and short-chain fatty acids (SCFAs). The current study emphasises the relationship of the gut-brain axis with cognitive performance and elucidates the underlying biological components, with a focus on neurotransmitters such as serotonin, indole derivatives, and catecholamine. These biological components play important roles in both the digestive and brain systems. Recent research has linked the gut microbiome to a variety of cognitive disorders, including Alzheimer's (AD). The review describes the intriguing role of the gut-brain axis in recognition memory depending on local network connections within the hippocampal as well as other additional hippocampal portions of the Papez circuit. The available data from various research papers show how the gut microbiota might alter brain function and hence psychotic and cognitive illnesses. The role of supplementary probiotics is emphasized for the reduction of brain-related dysfunction as a viable strategy in handling cognitive disorders. Further, the study elucidates the mode of action of probiotics with reported adverse effects.

Keywords: Gut microbiota, Gut-brain axis, Alzheimer’s disease, Papez circuit, Cognition, Probiotics.

Graphical Abstract

[1]
Kho ZY, Lal SK. The human gut microbiome–a potential controller of wellness and disease. Front Microbiol 2018; 9: 1835.
[http://dx.doi.org/10.3389/fmicb.2018.01835] [PMID: 30154767]
[2]
Generoso JS, Giridharan VV, Lee J, Macedo D, Barichello T. The role of the microbiota-gut-brain axis in neuropsychiatric disorders. Br J Psychiatry 2021; 43(3): 293-305.
[http://dx.doi.org/10.1590/1516-4446-2020-0987] [PMID: 32667590]
[3]
Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558(Pt 1): 263-75.
[http://dx.doi.org/10.1113/jphysiol.2004.063388] [PMID: 15133062]
[4]
Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol 2015; 28(2): 203-9.
[PMID: 25830558]
[5]
Mittal R, Debs LH, Patel AP, et al. Neurotransmitters: The Critical Modulators Regulating Gut-Brain Axis. J Cell Physiol 2017; 232(9): 2359-72.
[http://dx.doi.org/10.1002/jcp.25518] [PMID: 27512962]
[6]
Aggleton JP, Nelson AJ. Why do lesions in the rodent anterior thalamic nuclei cause such severe spatial deficits? Neurosci Biobehav Rev 2015; 54: 131-44.
[http://dx.doi.org/10.1016/j.neubiorev.2014.08.013] [PMID: 25195980]
[7]
Lyte M. Microbial endocrinology and the microbiota-gut-brain axis. Adv Exp Med Biol 2014; 817: 3-24.
[http://dx.doi.org/10.1007/978-1-4939-0897-4_1] [PMID: 24997027]
[8]
Vernocchi P, Del Chierico F, Putignani L. Gut microbiota profiling: Metabolomics based approach to unravel compounds affecting human health. Front Microbiol 2016; 7: 1144.
[http://dx.doi.org/10.3389/fmicb.2016.01144] [PMID: 27507964]
[9]
Clarke CJ, Haselden JN. Metabolic profiling as a tool for understanding mechanisms of toxicity. Toxicol Pathol 2008; 36(1): 140-7.
[http://dx.doi.org/10.1177/0192623307310947] [PMID: 18337232]
[10]
Zhao Y, Lukiw WJ. Microbiome-Mediated Upregulation of MicroRNA-146a in Sporadic Alzheimer’s Disease. Front Neurol 2018; 9: 145.
[http://dx.doi.org/10.3389/fneur.2018.00145] [PMID: 29615954]
[11]
Adamu L, Edeghagba B, Olatomi F, Ezeokoli O, Elijah A. Microorganisms associated with commercial motorcycle helmets in Lagos metropolis. J Microbiol Biotechnol Food Sci 2021; 2021: 1179-88.
[12]
Laterza L, Rizzatti G, Gaetani E, Chiusolo P, Gasbarrini A. The gut microbiota and immune system relationship in human graftversus-host disease. Mediterr J Hematol Infect Dis 2016; 8(1): e2016025.
[http://dx.doi.org/10.4084/mjhid.2016.025] [PMID: 27158438]
[13]
Arumugam M, Raes J, Pelletier E, et al. Erratum: Enterotypes of the human gut microbiome (Nature (2011) 473 (174-180)). Nature 2011; 474: 666.
[http://dx.doi.org/10.1038/nature10187]
[14]
Washabau RJ, Day MJ. Canine and feline gastroenterology. Elsevier Health Sciences 2012.
[15]
Petra AI, Panagiotidou S, Hatziagelaki E, Stewart JM, Conti P, Theoharides TC. Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther 2015; 37(5): 984-95.
[http://dx.doi.org/10.1016/j.clinthera.2015.04.002] [PMID: 26046241]
[16]
Moco S, Collino S, Rezzi S, Martin FP. Metabolomics perspectives in pediatric research. Pediatr Res 2013; 73(4 Pt 2): 570-6.
[http://dx.doi.org/10.1038/pr.2013.1] [PMID: 23314292]
[17]
Putignani L, Del Chierico F, Vernocchi P, et al. Gut microbiota dysbiosis as risk and premorbid factors of IBD and IBS along the childhood–adulthood transition. Inflamm Bowel Dis 2016; 22(2): 487-504.
[http://dx.doi.org/10.1097/MIB.0000000000000602] [PMID: 26588090]
[18]
de J R De-Paula V, Forlenza AS, Forlenza OV. Relevance of gutmicrobiota in cognition, behaviour and Alzheimer’s disease. Pharmacol Res 2018; 136: 29-34.
[http://dx.doi.org/10.1016/j.phrs.2018.07.007] [PMID: 30138667]
[19]
Tsigos C, Chrousos GP. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 2002; 53(4): 865-71.
[http://dx.doi.org/10.1016/S0022-3999(02)00429-4] [PMID: 12377295]
[20]
Mayer EA, Savidge T, Shulman RJ. Brain-gut microbiome interactions and functional bowel disorders. Gastroenterology 2014; 146(6): 1500-12.
[http://dx.doi.org/10.1053/j.gastro.2014.02.037] [PMID: 24583088]
[21]
Sharkey KA, Mawe GM. Neuroimmune and epithelial interactions in intestinal inflammation. Curr Opin Pharmacol 2002; 2(6): 669-77.
[http://dx.doi.org/10.1016/S1471-4892(02)00215-1] [PMID: 12482729]
[22]
Dinan TG, Cryan JF. Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 2012; 37(9): 1369-78.
[http://dx.doi.org/10.1016/j.psyneuen.2012.03.007] [PMID: 22483040]
[23]
Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405(6785): 458-62.
[http://dx.doi.org/10.1038/35013070] [PMID: 10839541]
[24]
Magro F, Vieira-Coelho MA, Fraga S, et al. Impaired synthesis or cellular storage of norepinephrine, dopamine, and 5-hydroxytryptamine in human inflammatory bowel disease. Dig Dis Sci 2002; 47(1): 216-24.
[http://dx.doi.org/10.1023/A:1013256629600] [PMID: 11837726]
[25]
Clarke G, Grenham S, Scully P, et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 2013; 18(6): 666-73.
[http://dx.doi.org/10.1038/mp.2012.77] [PMID: 22688187]
[26]
Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI. Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001; 291(5505): 881-4.
[http://dx.doi.org/10.1126/science.291.5505.881] [PMID: 11157169]
[27]
Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol Behav 2009; 96(4-5): 557-67.
[http://dx.doi.org/10.1016/j.physbeh.2008.12.004] [PMID: 19135464]
[28]
Walker JR, Ediger JP, Graff LA, et al. The Manitoba IBD cohort study: A population-based study of the prevalence of lifetime and 12-month anxiety and mood disorders. Am J Gastroenterol 2008; 103(8): 1989-97.
[http://dx.doi.org/10.1111/j.1572-0241.2008.01980.x] [PMID: 18796096]
[29]
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(4): 1179-88.
[http://dx.doi.org/10.1016/j.neuroscience.2010.08.005] [PMID: 20696216]
[30]
Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 2012; 10(11): 735-42.
[http://dx.doi.org/10.1038/nrmicro2876] [PMID: 23000955]
[31]
Oberauer K. How to say no: single- and dual-process theories of short-term recognition tested on negative probes. J Exp Psychol Learn Mem Cogn 2008; 34(3): 439-59.
[http://dx.doi.org/10.1037/0278-7393.34.3.439] [PMID: 18444748]
[32]
Mather G. Foundations of sensation and perception. USA: Psychol Press 2016.
[http://dx.doi.org/10.4324/9781315672236]
[33]
Gareau MG, Sherman PM, Walker WA. Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 2010; 7(9): 503-14.
[http://dx.doi.org/10.1038/nrgastro.2010.117] [PMID: 20664519]
[34]
Gareau MG, Wine E, Rodrigues DM, et al. Bacterial infection causes stress-induced memory dysfunction in mice. Gut 2011; 60(3): 307-17.
[http://dx.doi.org/10.1136/gut.2009.202515] [PMID: 20966022]
[35]
Matsumoto M, Kibe R, Ooga T, et al. Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study. Front Syst Neurosci 2013; 7: 9.
[http://dx.doi.org/10.3389/fnsys.2013.00009] [PMID: 23630473]
[36]
O’Brien ME, Anderson H, Kaukel E, et al. SRL172 (killed Mycobacterium vaccae) in addition to standard chemotherapy improves quality of life without affecting survival, in patients with advanced non-small-cell lung cancer: Phase III results. Ann Oncol 2004; 15(6): 906-14.
[http://dx.doi.org/10.1093/annonc/mdh220] [PMID: 15151947]
[37]
Carlson AL, Xia K, Azcarate-Peril MA, et al. Infant gut microbiome associated with cognitive development. Biol Psychiatry 2018; 83(2): 148-59.
[http://dx.doi.org/10.1016/j.biopsych.2017.06.021] [PMID: 28793975]
[38]
Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA. Development of the preterm infant gut microbiome: A research priority. Microbiome 2014; 2: 38.
[http://dx.doi.org/10.1186/2049-2618-2-38] [PMID: 25332768]
[39]
Tognini P. Gut Microbiota: A potential regulator of neurodevelopment. Front Cell Neurosci 2017; 11: 25.
[http://dx.doi.org/10.3389/fncel.2017.00025] [PMID: 28223922]
[40]
Hollister EB, Riehle K, Luna RA, et al. Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome 2015; 3: 36.
[http://dx.doi.org/10.1186/s40168-015-0101-x] [PMID: 26306392]
[41]
Kametani F, Hasegawa M. Reconsideration of Amyloid Hypothesis and Tau Hypothesis in Alzheimer’s Disease. Front Neurosci 2018; 12: 25.
[http://dx.doi.org/10.3389/fnins.2018.00025] [PMID: 29440986]
[42]
Nagpal R, Neth BJ, Wang S, Craft S, Yadav H. Modified Mediterranean-ketogenic diet modulates gut microbiome and short-chain fatty acids in association with Alzheimer’s disease markers in subjects with mild cognitive impairment. EBioMedicine 2019; 47: 529-42.
[http://dx.doi.org/10.1016/j.ebiom.2019.08.032] [PMID: 31477562]
[43]
Brandscheid C, Schuck F, Reinhardt S, et al. Altered Gut Microbiome Composition and Tryptic Activity of the 5xFAD Alzheimer’s Mouse Model. J Alzheimers Dis 2017; 56(2): 775-88.
[http://dx.doi.org/10.3233/JAD-160926] [PMID: 28035935]
[44]
Proctor C, Thiennimitr P, Chattipakorn N, Chattipakorn SC. Diet, gut microbiota and cognition. Metab Brain Dis 2017; 32(1): 1-17.
[http://dx.doi.org/10.1007/s11011-016-9917-8] [PMID: 27709426]
[45]
Saiyasit N, Chunchai T, Prus D, et al. Gut dysbiosis develops before metabolic disturbance and cognitive decline in high-fat diet-induced obese condition. Nutrition 2020; 69: 110576.
[http://dx.doi.org/10.1016/j.nut.2019.110576] [PMID: 31580986]
[46]
Desmedt O, Broers VJV, Zamariola G, Pachikian B, Delzenne N, Luminet O. Effects of prebiotics on affect and cognition in human intervention studies. Nutr Rev 2019; 77(2): 81-95.
[http://dx.doi.org/10.1093/nutrit/nuy052] [PMID: 30535275]
[47]
Roman P, Estévez AF, Miras A, et al. A pilot randomized controlled trial to explore cognitive and emotional effects of probiotics in fibromyalgia. Sci Rep 2018; 8(1): 10965.
[http://dx.doi.org/10.1038/s41598-018-29388-5] [PMID: 30026567]
[48]
Sahar T, Shalev AY, Porges SW. Vagal modulation of responses to mental challenge in posttraumatic stress disorder. Biol Psychiatry 2001; 49(7): 637-43.
[http://dx.doi.org/10.1016/S0006-3223(00)01045-3] [PMID: 11297721]
[49]
Bravo JA, Forsythe P, Chew MV, 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.
[http://dx.doi.org/10.1073/pnas.1102999108] [PMID: 21876150]
[50]
Strigo IA, Craig AD. Interoception, homeostatic emotions and sympathovagal balance. Philos Trans R Soc Lond B Biol Sci 2016; 371(1708): 20160010.
[http://dx.doi.org/10.1098/rstb.2016.0010] [PMID: 28080968]
[51]
Huffman WJ, Subramaniyan S, Rodriguiz RM, Wetsel WC, Grill WM, Terrando N. Modulation of neuroinflammation and memory dysfunction using percutaneous vagus nerve stimulation in mice. Brain Stimul 2019; 12(1): 19-29.
[http://dx.doi.org/10.1016/j.brs.2018.10.005] [PMID: 30337243]
[52]
De Vadder F, Kovatcheva-Datchary P, Goncalves D, et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 2014; 156(1-2): 84-96.
[http://dx.doi.org/10.1016/j.cell.2013.12.016] [PMID: 24412651]
[53]
Li Y, Hao Y, Zhu J, Owyang C. Serotonin released from intestinal enterochromaffin cells mediates luminal non-cholecystokinin-stimulated pancreatic secretion in rats. Gastroenterology 2000; 118(6): 1197-207.
[http://dx.doi.org/10.1016/S0016-5085(00)70373-8] [PMID: 10833495]
[54]
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.
[http://dx.doi.org/10.1016/j.neuroimage.2015.11.018] [PMID: 26577887]
[55]
Terbeck S, Savulescu J, Chesterman LP, Cowen PJ. Noradrenaline effects on social behaviour, intergroup relations, and moral decisions. Neurosci Biobehav Rev 2016; 66: 54-60.
[http://dx.doi.org/10.1016/j.neubiorev.2016.03.031] [PMID: 27126289]
[56]
Lyte M. Microbial endocrinology: Host-microbiota neuroendocrine interactions influencing brain and behavior. Gut Microbes 2014; 5(3): 381-9.
[http://dx.doi.org/10.4161/gmic.28682] [PMID: 24690573]
[57]
Pokusaeva K, Johnson C, Luk B, et al. GABA-producing Bifidobacterium dentium modulates visceral sensitivity in the intestine. Neurogastroenterol Motil 2017; 29(1): e12904.
[http://dx.doi.org/10.1111/nmo.12904] [PMID: 27458085]
[58]
Yu X, Ye Z, Houston CM, et al. Wakefulness is governed by GABA and histamine cotransmission. Neuron 2015; 87(1): 164-78.
[http://dx.doi.org/10.1016/j.neuron.2015.06.003] [PMID: 26094607]
[59]
Lamas B, Natividad JM, Sokol H. Aryl hydrocarbon receptor and intestinal immunity. Mucosal Immunol 2018; 11(4): 1024-38.
[http://dx.doi.org/10.1038/s41385-018-0019-2] [PMID: 29626198]
[60]
Cohen LJ, Kang HS, Chu J, et al. Functional metagenomic discovery of bacterial effectors in the human microbiome and isolation of commendamide, a GPCR G2A/132 agonist. Proc Natl Acad Sci USA 2015; 112(35): E4825-34.
[http://dx.doi.org/10.1073/pnas.1508737112] [PMID: 26283367]
[61]
Cryan JF, O’Riordan KJ, Sandhu K, Peterson V, Dinan TG. The gut microbiome in neurological disorders. Lancet Neurol 2020; 19(2): 179-94.
[http://dx.doi.org/10.1016/S1474-4422(19)30356-4] [PMID: 31753762]
[62]
Bistoletti M, Caputi V, Baranzini N, et al. Antibiotic treatment-induced dysbiosis differently affects BDNF and TrkB expression in the brain and in the gut of juvenile mice. PLoS One 2019; 14(2): e0212856.
[http://dx.doi.org/10.1371/journal.pone.0212856] [PMID: 30794676]
[63]
Bourassa MW, Alim I, Bultman SJ, Ratan RR. Butyrate, neuroepigenetics and the gut microbiome: Can a high fiber diet improve brain health? Neurosci Lett 2016; 625: 56-63.
[http://dx.doi.org/10.1016/j.neulet.2016.02.009] [PMID: 26868600]
[64]
Golubeva AV, Joyce SA, Moloney G, et al. Microbiota-related changes in bile acid & tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism. EBioMedicine 2017; 24: 166-78.
[http://dx.doi.org/10.1016/j.ebiom.2017.09.020] [PMID: 28965876]
[65]
Shah A, Jhawar SS, Goel A. Analysis of the anatomy of the Papez circuit and adjoining limbic system by fiber dissection techniques. J Clin Neurosci 2012; 19(2): 289-98.
[http://dx.doi.org/10.1016/j.jocn.2011.04.039] [PMID: 22209397]
[66]
Sun Y, Sommerville NR, Liu JYH, et al. Intra-gastrointestinal amyloid-β1-42 oligomers perturb enteric function and induce Alzheimer’s disease pathology. J Physiol 2020; 598(19): 4209-23.
[http://dx.doi.org/10.1113/JP279919] [PMID: 32617993]
[67]
Cattaneo A, Cattane N, Galluzzi S, et al. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging 2017; 49: 60-8.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.08.019] [PMID: 27776263]
[68]
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 microbiome-gut-brain axis. Neuroscience 2013; 240: 287-96.
[http://dx.doi.org/10.1016/j.neuroscience.2013.02.055] [PMID: 23500100]
[69]
Kobayashi T, Suzuki T, Kaji R, et al. Probiotic upregulation of peripheral IL-17 responses does not exacerbate neurological symptoms in experimental autoimmune encephalomyelitis mouse models. Immunopharmacol Immunotoxicol 2012; 34(3): 423-33.
[http://dx.doi.org/10.3109/08923973.2010.617755] [PMID: 21970527]
[70]
Nimgampalle M, Kuna Y. Anti-Alzheimer properties of probiotic, Lactobacillus plantarum MTCC 1325 in Alzheimer’s Disease induced albino rats. J Clin Diagn Res 2017; 11(8): KC01-5.
[http://dx.doi.org/10.7860/JCDR/2017/26106.10428] [PMID: 28969160]
[71]
Ohland CL, Kish L, Bell H, et al. Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology 2013; 38(9): 1738-47.
[http://dx.doi.org/10.1016/j.psyneuen.2013.02.008] [PMID: 23566632]
[72]
Athari Nik Azm S, Djazayeri A, Safa M, et al. Lactobacilli and bifidobacteria ameliorate memory and learning deficits and oxidative stress in β-amyloid (1-42) injected rats. Appl Physiol Nutr Metab 2018; 43(7): 718-26.
[http://dx.doi.org/10.1139/apnm-2017-0648] [PMID: 29462572]
[73]
Liu J, Sun J, Wang F, et al. Neuroprotective effects of clostridium butyricum against vascular dementia in mice via metabolic butyrate. BioMed Res Int 2015; 2015: 412946.
[http://dx.doi.org/10.1155/2015/412946] [PMID: 26523278]
[74]
Bonfili L, Cecarini V, Berardi S, et al. Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels. Sci Rep 2017; 7(1): 2426.
[http://dx.doi.org/10.1038/s41598-017-02587-2] [PMID: 28546539]
[75]
Kobayashi Y, Sugahara H, Shimada K, et al. Therapeutic potential of Bifidobacterium breve strain A1 for preventing cognitive impairment in Alzheimer’s disease. Sci Rep 2017; 7(1): 13510.
[http://dx.doi.org/10.1038/s41598-017-13368-2] [PMID: 29044140]
[76]
Xin Y, Diling C, Jian Y, et al. Effects of Oligosaccharides From Morinda officinalis on gut microbiota and metabolome of APP/PS1 transgenic mice. Front Neurol 2018; 9: 412.
[http://dx.doi.org/10.3389/fneur.2018.00412] [PMID: 29962999]
[77]
Ko CY, Lin H-TV, Tsai GJ. Gamma-aminobutyric acid production in black soybean milk by Lactobacillus brevis FPA 3709 and the antidepressant effect of the fermented product on a forced swimming rat model. Process Biochem 2013; 48: 559-68.
[http://dx.doi.org/10.1016/j.procbio.2013.02.021]
[78]
Forslund K, Hildebrand F, Nielsen T, et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 2015; 528(7581): 262-6.
[http://dx.doi.org/10.1038/nature15766] [PMID: 26633628]
[79]
Chen SG, Stribinskis V, Rane MJ, et al. Exposure to the functional bacterial amyloid protein curli enhances alpha-synuclein aggregation in aged fischer 344 rats and Caenorhabditis elegans. Sci Rep 2016; 6: 34477.
[http://dx.doi.org/10.1038/srep34477] [PMID: 27708338]
[80]
Allen AP, Hutch W, Borre YE, et al. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl Psychiatry 2016; 6(11): e939-.
[http://dx.doi.org/10.1038/tp.2016.191] [PMID: 27801892]
[81]
Anderson JR, Carroll I, Azcarate-Peril MA, et al. A preliminary examination of gut microbiota, sleep, and cognitive flexibility in healthy older adults. Sleep Med 2017; 38: 104-7.
[http://dx.doi.org/10.1016/j.sleep.2017.07.018] [PMID: 29031742]
[82]
Osadchiy V, Labus JS, Gupta A, et al. Correlation of tryptophan metabolites with connectivity of extended central reward network in healthy subjects. PLoS One 2018; 13(8): e0201772.
[http://dx.doi.org/10.1371/journal.pone.0201772] [PMID: 30080865]
[83]
Labus JS, Hollister EB, Jacobs J, et al. Differences in gut microbial composition correlate with regional brain volumes in irritable bowel syndrome. Microbiome 2017; 5(1): 49.
[http://dx.doi.org/10.1186/s40168-017-0260-z] [PMID: 28457228]
[84]
Bagga D, Reichert JL, Koschutnig K, et al. Probiotics drive gut microbiome triggering emotional brain signatures. Gut Microbes 2018; 9(6): 486-96.
[http://dx.doi.org/10.1080/19490976.2018.1460015] [PMID: 29723105]
[85]
Lew L-C, Hor Y-Y, Yusoff NAA, et al. Probiotic Lactobacillus plantarum P8 alleviated stress and anxiety while enhancing memory and cognition in stressed adults: A randomised, double-blind, placebo-controlled study. Clin Nutr 2019; 38(5): 2053-64.
[http://dx.doi.org/10.1016/j.clnu.2018.09.010] [PMID: 30266270]
[86]
Tillisch K, Labus J, Kilpatrick L, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 2013; 144(7): 1394-401.
[http://dx.doi.org/10.1053/j.gastro.2013.02.043] [PMID: 23474283]
[87]
Kelly JR, Allen AP, Temko A, et al. Lost in translation? The potential psychobiotic Lactobacillus rhamnosus (JB-1) fails to modulate stress or cognitive performance in healthy male subjects. Brain Behav Immun 2017; 61: 50-9.
[http://dx.doi.org/10.1016/j.bbi.2016.11.018] [PMID: 27865949]
[88]
Bagga D, Aigner CS, Reichert JL, et al. Influence of 4-week multi-strain probiotic administration on resting-state functional connectivity in healthy volunteers. Eur J Nutr 2019; 58(5): 1821-7.
[http://dx.doi.org/10.1007/s00394-018-1732-z] [PMID: 29850990]
[89]
Lv T, Ye M, Luo F, et al. Probiotics treatment improves cognitive impairment in patients and animals: A systematic review and meta-analysis. Neurosci Biobehav Rev 2021; 120: 159-72.
[http://dx.doi.org/10.1016/j.neubiorev.2020.10.027] [PMID: 33157148]
[90]
Pedersen BK, Saltin B. Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports 2015; 25 (Suppl. 3): 1-72. [1].
[http://dx.doi.org/10.1111/sms.12581] [PMID: 26606383]
[91]
Ticinesi A, Tana C, Nouvenne A, Prati B, Lauretani F, Meschi T. Gut microbiota, cognitive frailty and dementia in older individuals: A systematic review. Clin Interv Aging 2018; 13: 1497-511.
[http://dx.doi.org/10.2147/CIA.S139163] [PMID: 30214170]
[92]
Gentile CL, Weir TL. The gut microbiota at the intersection of diet and human health. Science 2018; 362(6416): 776-80.
[http://dx.doi.org/10.1126/science.aau5812] [PMID: 30442802]
[93]
Suganya K, Koo B-S. Gut-Brain axis: Role of gut microbiota on neurological disorders and how probiotics/prebiotics beneficially modulate microbial and immune pathways to improve brain functions. Int J Mol Sci 2020; 21(20): 7551.
[http://dx.doi.org/10.3390/ijms21207551] [PMID: 33066156]
[94]
Rezaei Asl Z, Sepehri G, Salami M. Probiotic treatment improves the impaired spatial cognitive performance and restores synaptic plasticity in an animal model of Alzheimer’s disease. Behav Brain Res 2019; 376: 112183.
[http://dx.doi.org/10.1016/j.bbr.2019.112183] [PMID: 31472194]
[95]
Mehrabadi S, Sadr SS. Assessment of probiotics mixture on memory function, inflammation markers, and oxidative stress in an Alzheimer’s Disease model of rats. Iran Biomed J 2020; 24(4): 220-8.
[http://dx.doi.org/10.29252/ibj.24.4.220] [PMID: 32306720]
[96]
Huang H, Xu H, Luo Q, et al. Fecal microbiota transplantation to treat Parkinson’s disease with constipation: A case report. Medicine (Baltimore) 2019; 98(26): e16163.
[http://dx.doi.org/10.1097/MD.0000000000016163] [PMID: 31261545]
[97]
St Laurent R, O’Brien LM, Ahmad ST. Sodium butyrate improves locomotor impairment and early mortality in a rotenone-induced Drosophila model of Parkinson’s disease. Neuroscience 2013; 246: 382-90.
[http://dx.doi.org/10.1016/j.neuroscience.2013.04.037] [PMID: 23623990]
[98]
Campbell JM, Bellman SM, Stephenson MD, Lisy K. Metformin reduces all-cause mortality and diseases of ageing independent of its effect on diabetes control: A systematic review and meta-analysis. Ageing Res Rev 2017; 40: 31-44.
[http://dx.doi.org/10.1016/j.arr.2017.08.003] [PMID: 28802803]
[99]
de la Cuesta-Zuluaga J, Mueller NT, Corrales-Agudelo V, et al. Metformin is associated with higher relative abundance of mucin-degrading Akkermansia muciniphila and several short-chain fatty acid-producing microbiota in the gut. Diabetes Care 2017; 40(1): 54-62.
[http://dx.doi.org/10.2337/dc16-1324] [PMID: 27999002]
[100]
Hescham S, Jahanshahi A, Meriaux C, Lim LW, Blokland A, Temel Y. Behavioral effects of deep brain stimulation of different areas of the Papez circuit on memory- and anxiety-related functions. Behav Brain Res 2015; 292: 353-60.
[http://dx.doi.org/10.1016/j.bbr.2015.06.032] [PMID: 26119240]
[101]
Hescham S, Lim LW, Jahanshahi A, Blokland A, Temel Y. Deep brain stimulation in dementia-related disorders. Neurosci Biobehav Rev 2013; 37(10 Pt 2): 2666-75.
[http://dx.doi.org/10.1016/j.neubiorev.2013.09.002] [PMID: 24060532]