Gut microbiome-brain axis and inflammation in temperament, personality and psychopathology

https://doi.org/10.1016/j.cobeha.2022.101101Get rights and content

Highlights

  • Microbiome is associated with temperament from birth through childhood.

  • Associations have been observed between adult personality traits and gut microbiome.

  • Further work is needed to delineate the direction of these relationships.

  • Enrichment of microbiota affect mood and some psychopathologies.

  • Further work will determine whether microbiota enrichment affects personality traits.

Full understanding of temperament, personality and psychopathology must consider biological mechanisms beyond the brain. Over 4000 species of commensurate microbiota inhabit our bodies and influence almost all aspects of human physiological function. Evidence supports bidirectional relationships between the gut microbiome and brain function. For example, gut environment directly influences limbic function via the vagal nerve, modulating affect and stress-responsivity. In turn, states of distress affect the ecology of the gut, physiologically and through behavioural alteration (diet, social interaction). Furthermore, the gut microbiome modulates the release of inflammatory molecules and hormones, indirectly affecting brain structure and function. Thus, development of gut microbiome from gestation, through birth, during childhood, adulthood and into old age is associated with temperament, personality and psychological wellbeing, including sexual differentiation in psychological function during puberty, and vulnerability to developmental, psychiatric and neurological disorders. Moreover, nutrients known to affect gut function and inflammation (e.g. fatty acids) are associated with temperament and personality in clinical and nonclinical groups. These relationships may reflect the influence of psychological traits on the microbiome by determining how an organism explores the environment, seeks reward, its social interaction and food preferences. However, it might also reflect an effect of microbiome status on psychological function. There is a need for further systematic multidisciplinary studies that integrate psychology, neurosciences, immunology and microbiology to determine the direction of these relationships and fully understand the biological basis of temperament, personality and psychopathology.

Introduction

Substantial advances in understanding brain networks underpinning temperament, personality5 and psychopathology have been made over the last few decades [1,2]. However, recent evidence suggests that a full understanding of what makes us ‘us’ may require consideration of biological mechanisms beyond the brain [3••,4]. Over 4000 commensurate microbiota species inhabit our bodies, influencing almost all aspects of human physiological function. Indeed, only 1% of the combined human and microbial DNA in our bodies is human. Given temperament and personality affect perceived threat (Neuroticism), social (Extraversion) and environmental (Openness) interaction, the resulting physiological and behavioural changes may influence the gut microbiome (i.e. the gut microbial community, including genetic components, microbial biodiversity, and their resulting functionality) [5]. This, in part, contributes to the remarkable individual differences in gut microbiome diversity and composition, which influences physical and psychological health [3••,6]. In turn, the gut microbiota might also influence temperament and personality, via bidirectional communication with the brain [3••,7], involving both direct (cranial nerve X) and indirect (e.g. via immune and endocrine systems) pathways [8]. Thus, the gut and its microbial community may represent a missing link between psychological traits and health. The current manuscript reviews evidence in this field that is rapidly gaining ground in neuroscience, psychology and mental health [9].

Section snippets

Gut microbiome development

The gut contains 1013 microorganisms with over 1000 unique bacterial species, comprising four major phyla: Firmicutes (e.g. Lactobacillus, Lachnospira, Veillonella, Eubacterium, Roseburia, Ruminococcus), Bacteroidetes (e.g. Bacteroides, Parabacteroides), Actinobacteria (e.g. Bifidobacterium) and Proteobacteria (several gram-negative pathogens e.g. EscherichiaShigella, Gammaproteobacteria). Infants receive the majority of their initial microbiome via the mother during, and possibly before,

Microbiome and early life temperament

Regarding infant (18–27 months) temperament [20], microbiome phylogenetic diversity is associated with Surgency/Extraversion [21]. In boys only, Surgency/Extraversion has been associated with overall diversity and relative abundances of certain Firmicutes (Dialister, Ruminococcaceae) and Bacteroidetes (Rikenellaceae, Parabacteroides). This latter finding was in part associated with age and diet, while the relationship between phylogenetic diversity and Surgency (Extraversion) seemed unaffected

Microbiome and personality in adults

Regarding adult personality, Gammaproteobacteria (mostly pathogenic, including Escherichia coli) has been associated with Neuroticism (in line with inflammatory models of neuroticism), and indeed major depressive disorder [34,35], whilst Conscientiousness was characterised by lower Proteobacteria, and higher Lachnospiraceae (butyrate-producing bacteria related to anti-inflammatory mechanisms) [36]. Bacterial diversity has been associated with openness and agreeableness, which may reflect a

Microbiome, limbic and executive function

The varied relationship between gut microbiota and negative emotionality or fear with age may reflect differential subregion development of limbic networks involved in the response to threat, including those centred around the frontal-medial temporal connections [38] and neuroendocrine systems (i.e. hypothalamus-pituitary-adrenal axis [8]). Whilst development of limbic regions (e.g. amygdala) begins soon after conception, progressive structural and functional segregation between subregions’

Inflammation

As well as being the principal armament of our physiological defence system, adaptive inflammation collaborates with the microbiome to affect registration of environmental threats and opportunities, biasing perception to promote harm avoidance and facilitate recovery from illness [25]. Indeed, Gassen and Hill [25] suggest a specific adaptive role for inflammation in ‘social’ perception (punishment and reward) and associated personality traits. For example, the immune system has been

Endocrine function

Complex relationships exist between the endocrine, enteric and immune systems that influence psychological and physical health [78,79]. Hormones likely act as bidirectional conduits of communication between the microbiome and brain, impacting temperament, personality and vulnerability to psychopathology [79]. For example, sex steroid hormone levels in humans are correlated with gut microbial composition and diversity [80], and animal studies show transference of gut microbiota from male to

Prebiotics and probiotics

With regard to clinical trials in humans, meta-analyses suggest that whilst probiotics [84] have a significant effect on mood in clinical populations [85], their effects in non-clinical populations remain unclear [85]. Nevertheless, some positive findings exist. For example, in Petrochemical workers, probiotic yogurt (Lactobacillus and Bifidobacterium species) or supplement with several species led to improvement in depression, anxiety and stress [86]. A prebiotic [87] intervention trial

Summary and conclusion

Whilst several associations have been identified between the gut microbiome, temperament, personality and psychopathology across the lifespan, the direction of these relationships are currently unknown. At least in part, however, they likely reflect a role for temperament and personality on diversity and composition of the microbiome by influencing social and environmental exploration during development. This may, in turn, influence vulnerability to physical and psychological clinical

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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