Online first
Original article
Published online: 2024-07-18
The fecal content of Veillonellaceae family bacteria correlates with cognitive parameters in young healthy human subjects
1
, 1, 1, 2
, 1, 1, 2
Abstract
Introduction: Several lines of evidence suggest that the composition of gut microbiota influences the central nervous system function. Previous studies demonstrated that gut microbiota composition can affect the mood, anxiety and cognitive performance. However, most of the research was focused on the animal models and older humans. Relatively limited number of reports examined the influence of gut microbiota on cognitive functions in young, healthy human subjects.
Material and methods: We examined the influence of gut microbiota composition on cognitive performance in 30 volunteers (24 females and 6 males; mean age 22.53 ± 1.97 yr.). In order to evaluate the cognitive performance in our subject we used three standard tests: Face/Name Association Test, Trial Making Test and Stroop Test. The composition of intestinal microbiota was determined in fecal samples using 16S rDNA V3-V4 regions analysis.
Results: The study demonstrated that the proportion of Veillonellaceae bacteria (phylum Firmicutes) in the subject’s fecal matter positive correlated with the results of one of the cognitive tests — Trial Making Test.
Conclusions: Our results indicate that bacteria from Veillonellaceae family may influence the level of some cognitive functions (namely executive ones). Our results are consistent with previous studies describing the potential impact of intestinal bacterial on cognitive performance.
Keywords: FirmicutesVeillonellaceaeexecutive functiongut microbiotagut-brain axisTrial Making Test
References
- Kiely K. Cognitive Function. Encyclopedia of Quality of Life and Well-Being Research. 2014: 974–978.
- Kempermann G, Kuhn HG, Gage FH. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci. 1998; 18(9): 3206–3212.
- Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci. 1996; 16(6): 2027–2033.
- van Praag H, Shubert T, Zhao C, et al. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci. 2005; 25(38): 8680–8685.
- van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999; 2(3): 266–270.
- Wise PM, Dubal DB, Wilson ME, et al. Estradiol is a neuroprotective factor in in vivo and in vitro models of brain injury. J Neurocytol. 2000; 29(5-6): 401–410.
- Tanapat P, Hastings NB, Reeves AJ, et al. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci. 1999; 19(14): 5792–5801.
- Nguyen JCD, Killcross AS, Jenkins TA. Obesity and cognitive decline: role of inflammation and vascular changes. Front Neurosci. 2014; 8: 375.
- Wang C, Chan JSY, Ren L, et al. Obesity Reduces Cognitive and Motor Functions across the Lifespan. Neural Plast. 2016; 2016: 2473081.
- Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol. 2009; 6(5): 306–314.
- Gareau MG. Cognitive Function and the Microbiome. Int Rev Neurobiol. 2016; 131: 227–246.
- Rogers GB, Keating DJ, Young RL, et al. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol Psychiatry. 2016; 21(6): 738–748.
- Bäckhed F, Roswall J, Peng Y, et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe. 2015; 17(5): 690–703.
- Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005; 308(5728): 1635–1638.
- Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012; 489(7415): 242–249.
- O'Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006; 7(7): 688–693.
- Sekirov I, Russell SL, Antunes LC, et al. Gut microbiota in health and disease. Physiol Rev. 2010; 90(3): 859–904.
- Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014; 16(7): 1024–1033.
- Ley RE. Obesity and the human microbiome. Curr Opin Gastroenterol. 2010; 26(1): 5–11.
- Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012; 490(7418): 55–60.
- Blumberg R, Powrie F. Microbiota, disease, and back to health: a metastable journey. Sci Transl Med. 2012; 4(137): 137rv7.
- Jeffery IB, O'Toole PW, Öhman L, et al. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut. 2012; 61(7): 997–1006.
- Tilg H, Adolph TE, Gerner RR, et al. The Intestinal Microbiota in Colorectal Cancer. Cancer Cell. 2018; 33(6): 954–964.
- Finegold SM, Dowd SE, Gontcharova V, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe. 2010; 16(4): 444–453.
- Naseribafrouei A, Hestad K, Avershina E, et al. Correlation between the human fecal microbiota and depression. Neurogastroenterol Motil. 2014; 26(8): 1155–1162.
- Saji N, Niida S, Murotani K, et al. Analysis of the relationship between the gut microbiome and dementia: a cross-sectional study conducted in Japan. Sci Rep. 2019; 9(1): 1008.
- Vogt NM, Kerby RL, Dill-McFarland KA, et al. Gut microbiome alterations in Alzheimer's disease. Sci Rep. 2017; 7(1): 13537.
- Bruce-Keller AJ, Salbaum JM, Luo M, et al. Obese-type gut microbiota induce neurobehavioral changes in the absence of obesity. Biol Psychiatry. 2015; 77(7): 607–615.
- Zhang S, Qian Y, Li Q, et al. Metabolic and Neural Mechanisms Underlying the Associations Between Gut and Cognition: A Large-Scale Functional Network Connectivity Study. Front Neurosci. 2021; 15: 750704.
- Fernandez-Real JM, Serino M, Blasco G, et al. Gut Microbiota Interacts With Brain Microstructure and Function. J Clin Endocrinol Metab. 2015; 100(12): 4505–4513.
- Leal G, Bramham CR, Duarte CB. BDNF and Hippocampal Synaptic Plasticity. Vitam Horm. 2017; 104: 153–195.
- Diaz Heijtz R, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011; 108(7): 3047–3052.
- Alaish SM, Smith AD, Timmons J, et al. Gut microbiota, tight junction protein expression, intestinal resistance, bacterial translocation and mortality following cholestasis depend on the genetic background of the host. Gut Microbes. 2013; 4(4): 292–305.
- Kelly JR, Kennedy PJ, Cryan JF, et al. Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci. 2015; 9: 392.
- Erny D, Hrabě de Angelis AL, Jaitin D, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015; 18(7): 965–977.
- Trollor JN, Smith E, Agars E, et al. The association between systemic inflammation and cognitive performance in the elderly: the Sydney Memory and Ageing Study. Age (Dordr). 2012; 34(5): 1295–1308.
- MacFabe DF, Cain DP, Rodriguez-Capote K, et al. Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav Brain Res. 2007; 176(1): 149–169.
- Barichello T, Generoso JS, Simões LR, et al. Sodium Butyrate Prevents Memory Impairment by Re-establishing BDNF and GDNF Expression in Experimental Pneumococcal Meningitis. Mol Neurobiol. 2015; 52(1): 734–740.
- Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013; 341(6145): 569–573.
- Fung TC, Olson CA, Hsiao EY. Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci. 2017; 20(2): 145–155.
- Zhang L, Wang Y, Xiayu X, et al. Altered Gut Microbiota in a Mouse Model of Alzheimer's Disease. J Alzheimers Dis. 2017; 60(4): 1241–1257.
- Nakamura YK, Janowitz C, Metea C, et al. Short chain fatty acids ameliorate immune-mediated uveitis partially by altering migration of lymphocytes from the intestine. Sci Rep. 2017; 7(1): 11745.
- Sperling RA, Bates JF, Cocchiarella AJ, et al. Encoding novel face-name associations: a functional MRI study. Hum Brain Mapp. 2001; 14(3): 129–139.
- Peterson BS, Skudlarski P, Gatenby JC, et al. An fMRI study of Stroop word-color interference: evidence for cingulate subregions subserving multiple distributed attentional systems. Biol Psychiatry. 1999; 45(10): 1237–1258.
- Tombaugh TN. Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol. 2004; 19(2): 203–214.
- Vogt NM, Kerby RL, Dill-McFarland KA, et al. Gut microbiome alterations in Alzheimer's disease. Sci Rep. 2017; 7(1): 13537.
- Manderino L, Carroll I, Azcarate-Peril MA, et al. Preliminary Evidence for an Association Between the Composition of the Gut Microbiome and Cognitive Function in Neurologically Healthy Older Adults. J Int Neuropsychol Soc. 2017; 23(8): 700–705.
- Huang Y, Shi X, Li Z, et al. Possible association of Firmicutes in the gut microbiota of patients with major depressive disorder. Neuropsychiatr Dis Treat. 2018; 14: 3329–3337.
- Bajaj JS, Ridlon JM, Hylemon PB, et al. Linkage of gut microbiome with cognition in hepatic encephalopathy. Am J Physiol Gastrointest Liver Physiol. 2012; 302(1): G168–G175.
- Wright G, Jalan R. Ammonia and inflammation in the pathogenesis of hepatic encephalopathy: Pandora's box? Hepatology. 2007; 46(2): 291–294.
- Kobayashi Y, Kuhara T, Oki M, et al. Effects of A1 on the cognitive function of older adults with memory complaints: a randomised, double-blind, placebo-controlled trial. Benef Microbes. 2019; 10(5): 511–520.
- Xiao J, Katsumata N, Bernier F, et al. Probiotic Bifidobacterium breve in Improving Cognitive Functions of Older Adults with Suspected Mild Cognitive Impairment: A Randomized, Double-Blind, Placebo-Controlled Trial. J Alzheimers Dis. 2020; 77(1): 139–147.
- Luck B, Engevik MA, Ganesh BP, et al. Bifidobacteria shape host neural circuits during postnatal development by promoting synapse formation and microglial function. Sci Rep. 2020; 10(1): 7737.
- 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.