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Abstract
The intestinal microbiota is increasingly recognized as a complex signaling network that impacts on many systems beyond the enteric system modulating, among others, cognitive functions including learning, memory and decision-making processes. This has led to the concept of a microbiota-driven gut–brain axis, reflecting a bidirectional interaction between the central nervous system and the intestine. A deficit in synaptic plasticity is one of the many changes that occurs with age. Specifically, the archetypal model of plasticity, long-term potentiation (LTP), is reduced in hippocampus of middle-aged and aged rats. Because the intestinal microbiota might change with age, we have investigated whether the age-related deficit in LTP might be attenuated by changing the composition of intestinal microbiota with VSL#3, a probiotic mixture comprising 8 Gram-positive bacterial strains. Here, we report that treatment of aged rats with VSL#3 induced a robust change in the composition of intestinal microbiota with an increase in the abundance of Actinobacteria and Bacterioidetes, which was reduced in control-treated aged rats. VSL#3 administration modulated the expression of a large group of genes in brain tissue as assessed by whole gene expression, with evidence of a change in genes that impact on inflammatory and neuronal plasticity processes. The age-related deficit in LTP was attenuated in VSL#3-treated aged rats and this was accompanied by a modest decrease in markers of microglial activation and an increase in expression of BDNF and synapsin. The data support the notion that intestinal microbiota can be manipulated to positively impact on neuronal function.
Highlights
Age-related changes in the brain contribute to the time-related deterioration in cognitive function
Analysis of intestinal microbiota composition At day 0, young control-treated rats (YC) and young rats treated with VLS#3 (YV) showed only 3 of the 4 most populated bacterial phyla, as Bacteroidetes were not detected (Figure 1A)
At day 42, samples from young VSL#3-treated rats (YV) showed the same microbiota composition as that of YC, as Bacteroidetes and Actinobacteria phyla increased (962.7% and 38611% respectively) while both Firmicutes and Proteobacteria decreased (2961.7% and 2469.1% respectively) (Figure 1B). These results indicate that microbiota spontaneously changed during the 6 week period of the experiment, and this effect was independent of VSL#3 administration
Summary
Age-related changes in the brain contribute to the time-related deterioration in cognitive function. The deterioration in cognitive function is manifest by poorer spatial learning [2], while the alterations at the level of the synapse are reflected by loss of plasticity, for example a poorer ability of animals to sustain long-term potentiation (LTP). When these age-related neuroinflammatory changes are attenuated by treating aged rats with polyunsaturated fatty acids [3], statins [4] or a combination of vitamin D and dexamethasone [5,6], LTP is partially restored. An increased expression of hippocampal BDNF has been associated with restoration of LTP in middle-aged rats [9]
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