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      The gut microbiome as a driver of individual variation in cognition and functional behaviour.

      Philosophical transactions of the Royal Society of London. Series B, Biological sciences

      The Royal Society

      animal personality, cognition, stress, microbiome, diet, behaviour

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          Abstract

          Research into proximate and ultimate mechanisms of individual cognitive variation in animal populations is a rapidly growing field that incorporates physiological, behavioural and evolutionary investigations. Recent studies in humans and laboratory animals have shown that the enteric microbial community plays a central role in brain function and development. The 'gut-brain axis' represents a multi-directional signalling system that encompasses neurological, immunological and hormonal pathways. In particular it is tightly linked with the hypothalamic-pituitary-adrenal axis (HPA), a system that regulates stress hormone release and influences brain development and function. Experimental examination of the microbiome through manipulation of diet, infection, stress and exercise, suggests direct effects on cognition, including learning and memory. However, our understanding of these processes in natural populations is extremely limited. Here, we outline how recent advances in predominantly laboratory-based microbiome research can be applied to understanding individual differences in cognition. Experimental manipulation of the microbiome across natal and adult environments will help to unravel the interplay between cognitive variation and the gut microbial community. Focus on individual variation in the gut microbiome and cognition in natural populations will reveal new insight into the environmental and evolutionary constraints that drive individual cognitive variation.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

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          Most cited references 70

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          Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors.

          In vertebrates, including humans, individuals harbor gut microbial communities whose species composition and relative proportions of dominant microbial groups are tremendously varied. Although external and stochastic factors clearly contribute to the individuality of the microbiota, the fundamental principles dictating how environmental factors and host genetic factors combine to shape this complex ecosystem are largely unknown and require systematic study. Here we examined factors that affect microbiota composition in a large (n = 645) mouse advanced intercross line originating from a cross between C57BL/6J and an ICR-derived outbred line (HR). Quantitative pyrosequencing of the microbiota defined a core measurable microbiota (CMM) of 64 conserved taxonomic groups that varied quantitatively across most animals in the population. Although some of this variation can be explained by litter and cohort effects, individual host genotype had a measurable contribution. Testing of the CMM abundances for cosegregation with 530 fully informative SNP markers identified 18 host quantitative trait loci (QTL) that show significant or suggestive genome-wide linkage with relative abundances of specific microbial taxa. These QTL affect microbiota composition in three ways; some loci control individual microbial species, some control groups of related taxa, and some have putative pleiotropic effects on groups of distantly related organisms. These data provide clear evidence for the importance of host genetic control in shaping individual microbiome diversity in mammals, a key step toward understanding the factors that govern the assemblages of gut microbiota associated with complex diseases.
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            Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses.

            Adverse early life events are associated with a maladaptive stress response system and might increase the vulnerability to disease in later life. Several disorders have been associated with early life stress, ranging from depression to irritable bowel syndrome. This makes the identification of the neurobiological substrates that are affected by adverse experiences in early life invaluable. The purpose of this study was to assess the effect of early life stress on the brain-gut axis. Male rat pups were stressed by separating them from their mothers for 3 hours daily between postnatal days 2-12. The control group was left undisturbed with their mothers. Behavior, immune response, stress sensitivity, visceral sensation, and fecal microbiota were analyzed. The early life stress increased the number of fecal boli in response to a novel stress. Plasma corticosterone was increased in the maternally separated animals. An increase in the systemic immune response was noted in the stressed animals after an in vitro lipopolysaccharide challenge. Increased visceral sensation was seen in the stressed group. There was an alteration of the fecal microbiota when compared with the control group. These results show that this form of early life stress results in an altered brain-gut axis and is therefore an important model for investigating potential mechanistic insights into stress-related disorders including depression and IBS.
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              The mentality of crows: convergent evolution of intelligence in corvids and apes.

              Discussions of the evolution of intelligence have focused on monkeys and apes because of their close evolutionary relationship to humans. Other large-brained social animals, such as corvids, also understand their physical and social worlds. Here we review recent studies of tool manufacture, mental time travel, and social cognition in corvids, and suggest that complex cognition depends on a "tool kit" consisting of causal reasoning, flexibility, imagination, and prospection. Because corvids and apes share these cognitive tools, we argue that complex cognitive abilities evolved multiple times in distantly related species with vastly different brain structures in order to solve similar socioecological problems.
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                Author and article information

                Journal
                30104431
                6107574
                10.1098/rstb.2017.0286

                animal personality, cognition, stress, microbiome, diet, behaviour

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