Enduring neurobehavioral effects induced by microbiota depletion during the adolescent period

Lach, Gilliard; Fülling, Christine; Bastiaanssen, Thomaz F.S.; Fouhy, Fiona; Donovan, Aoife; Ventura-Silva, Ana Paula; Stanton, Catherine; Dinan, Timothy G.; Cryan, John F.

doi:10.1038/s41398-020-01073-0

Cited by 44 publications

(38 citation statements)

References 94 publications

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“…The 2-week broad-spectrum antibiotic treatment caused a gut dysbiosis with specific changes in the cecal and fecal microbiota composition. Bacterial diversity and species evenness were decreased in antibiotic-treated animals, in agreement with various authors [ 60 , 61 , 62 ]. Additionally, this dysbiotic state was characterized by the reduction of the Firmicutes/Bacteroidetes (F/B) ratio and increases in Proteobacteria and Verrucomicrobia phyla.…”

Section: Discussionsupporting

confidence: 91%

Protective Effects of Probiotics on Cognitive and Motor Functions, Anxiety Level, Visceral Sensitivity, Oxidative Stress and Microbiota in Mice with Antibiotic-Induced Dysbiosis

Arslanova

Tarasova

Alexandrova

et al. 2021

Life

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Accumulating clinical and preclinical data indicate a prominent role of gut microbiota in regulation of physiological functions. The gut–brain axis imbalance due to gut dysbiosis is associated with a range of neurodegenerative diseases. Probiotics were suggested not only to restore intestinal dysbiosis but also modulate stress response and improve mood and anxiety symptoms. In this study, we assessed the effects of probiotic lactobacilli on behavioral reactions, the level of oxidative stress and microbiota content in mice administered to broad-spectrum antibiotics. Our study demonstrates that antibiotic treatment of adolescent mice for two weeks resulted in higher mortality and lower weight gain and induced significant changes in behavior including lower locomotor and exploratory activity, reduced muscle strength, visceral hypersensitivity, higher level of anxiety and impaired cognitive functions compared to the control group. These changes were accompanied by decreased diversity and total amount of bacteria, abundance of Proteobacteria and Verrucomicrobia phyla, and reduced Firmicutes/Bacteroides ratio in the gut microbiota. Moreover, a higher level of oxidative stress was found in brain and skeletal muscle tissues of mice treated with antibiotics. Oral administration of two Lactobacillus strains prevented the observed changes and improved not only microbiota content but also the behavioral alterations, suggesting a neuroprotective and antioxidant role of probiotics.

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Section: Discussionsupporting

confidence: 91%

Protective Effects of Probiotics on Cognitive and Motor Functions, Anxiety Level, Visceral Sensitivity, Oxidative Stress and Microbiota in Mice with Antibiotic-Induced Dysbiosis

Arslanova

Tarasova

Alexandrova

et al. 2021

Life

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“…Results showed a decrease of members of the family Lachnospiraceae and Bacteroides genus, which are also associated with anxiety in humans [ 42 ]. Furthermore, expression of genes involved in neurotransmission (such as Gabra1 , Gabbr1 , Npy, or Nr3c1 ), SCFA, and tight-junction proteins were more drastically affected during adolescence than adulthood [ 43 ]. These results highlight the consequences of gut microbiota manipulation during adolescence in mood disorders and the need for this kind of study in humans.…”

Section: Resultsmentioning

confidence: 99%

Effects of Microbiota Imbalance in Anxiety and Eating Disorders: Probiotics as Novel Therapeutic Approaches

Navarro-Tapia

Almeida-Toledano

Sebastiani

et al. 2021

IJMS

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Anxiety and eating disorders produce a physiological imbalance that triggers alterations in the abundance and composition of gut microbiota. Moreover, the gut–brain axis can be altered by several factors such as diet, lifestyle, infections, and antibiotic treatment. Diet alterations generate gut dysbiosis, which affects immune system responses, inflammation mechanisms, the intestinal permeability, as well as the production of short chain fatty acids and neurotransmitters by gut microbiota, which are essential to the correct function of neurological processes. Recent studies indicated that patients with generalized anxiety or eating disorders (anorexia nervosa, bulimia nervosa, and binge-eating disorders) show a specific profile of gut microbiota, and this imbalance can be partially restored after a single or multi-strain probiotic supplementation. Following the PRISMA methodology, the current review addresses the main microbial signatures observed in patients with generalized anxiety and/or eating disorders as well as the importance of probiotics as a preventive or a therapeutic tool in these pathologies.

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“…The gut microbiome has recently been implicated in modulating neurocognitive development and consequent functioning [1][2][3][4] . Early life developmental periods represent critical windows for the impact of indigenous gut microbes on the brain, as evidenced by the reversal of behavioral and neurochemical abnormalities in germ free rodents when inoculated with conventional microbiota during early life, but not during adulthood [5][6][7] .…”

Section: Introductionmentioning

confidence: 99%

“…2 University of California, Los Angeles, CA, USA. 3 University of Southern California, Los Angeles, CA, USA…”

mentioning

confidence: 99%

Gut microbial taxa elevated by dietary sugar disrupt memory function

et al. 2021

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Emerging evidence highlights a critical relationship between gut microbiota and neurocognitive development. Excessive consumption of sugar and other unhealthy dietary factors during early life developmental periods yields changes in the gut microbiome as well as neurocognitive impairments. However, it is unclear whether these two outcomes are functionally connected. Here we explore whether excessive early life consumption of added sugars negatively impacts memory function via the gut microbiome. Rats were given free access to a sugar-sweetened beverage (SSB) during the adolescent stage of development. Memory function and anxiety-like behavior were assessed during adulthood and gut bacterial and brain transcriptome analyses were conducted. Taxa-specific microbial enrichment experiments examined the functional relationship between sugar-induced microbiome changes and neurocognitive and brain transcriptome outcomes. Chronic early life sugar consumption impaired adult hippocampal-dependent memory function without affecting body weight or anxiety-like behavior. Adolescent SSB consumption during adolescence also altered the gut microbiome, including elevated abundance of two species in the genus Parabacteroides (P. distasonis and P. johnsonii) that were negatively correlated with hippocampal function. Transferred enrichment of these specific bacterial taxa in adolescent rats impaired hippocampal-dependent memory during adulthood. Hippocampus transcriptome analyses revealed that early life sugar consumption altered gene expression in intracellular kinase and synaptic neurotransmitter signaling pathways, whereas Parabacteroides microbial enrichment altered gene expression in pathways associated with metabolic function, neurodegenerative disease, and dopaminergic signaling. Collectively these results identify a role for microbiota “dysbiosis” in mediating the detrimental effects of early life unhealthy dietary factors on hippocampal-dependent memory function.

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Enduring neurobehavioral effects induced by microbiota depletion during the adolescent period

Cited by 44 publications

References 94 publications

Protective Effects of Probiotics on Cognitive and Motor Functions, Anxiety Level, Visceral Sensitivity, Oxidative Stress and Microbiota in Mice with Antibiotic-Induced Dysbiosis

Protective Effects of Probiotics on Cognitive and Motor Functions, Anxiety Level, Visceral Sensitivity, Oxidative Stress and Microbiota in Mice with Antibiotic-Induced Dysbiosis

Effects of Microbiota Imbalance in Anxiety and Eating Disorders: Probiotics as Novel Therapeutic Approaches

Gut microbial taxa elevated by dietary sugar disrupt memory function

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