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

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'.

Keywords: animal personality; behaviour; cognition; diet; microbiome; stress.

Figure 1.

Causes and consequences of individual variation in the microbiome in relation to environmental and developmental effects, and the subsequent impact on neurological, cognitive and behavioural traits. Arrows indicate potential causal directions of relationships and are not exhaustive (for example, development may directly affect cognition independent of microbiome). Italics refer to selected phenotypes that have yet to be investigated empirically (i.e. animal personality) and where null results have been found (i.e. social information transfer [18]).

Figure 2.

Positive feedback loops between microbiome diversity and cognition. A highly diverse microbiome improves memory and behavioural flexibility and associated foraging success, and as a result, dietary breadth maintains a diverse microbiome. By contrast, low microbial diversity impairs cognitive abilities, resulting in poor foraging success. However, the gut microbiome can influence host food preferences and reward valence as a means to increase microbial diversity, and to improve learning and memory for food sources, breaking out of the positive feedback loop (black arrow). Finally, individual differences in cognition (specificity versus generalization), competitive ability and innovativeness influence diet. Arrows represent directional influences on, or in response to, phenotypic traits (represented within grey boxes).