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Microbiota and the social brain

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Science  01 Nov 2019:
Vol. 366, Issue 6465, eaar2016
DOI: 10.1126/science.aar2016

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Animal sociability through microbes

Accumulating evidence suggests that the microbiota living in and on animals has important functions in the social architecture of those animals. Sherwin et al. review how the microbiota might facilitate neurodevelopment, help program social behaviors, and facilitate communication in various animal species, including humans. Understanding the complex relationship between microbiota and animal sociability may also identify avenues for treating social disorders in humans.

Science, this issue p. eaar2016

Structured Abstract

BACKGROUND

Increasingly, it is recognized that the microbes resident in the gastrointestinal tract can influence brain physiology and behavior. Research has shown that the gastrointestinal microbiota can signal to the brain via a diverse set of pathways, including immune activation, production of microbial metabolites and peptides, activation of the vagus nerve, and production of various neurotransmitters and neuromodulators in the gut itself. Collectively, this bidirectional pathway is known as the microbiota-gut-brain axis. In the absence of a microbiota, germ-free and antibiotic-treated mice exhibit alterations to several central physiological processes such as neurotransmitter turnover, neuroinflammation, neurogenesis, and neuronal morphology. Perhaps as a result of these neurological alterations, the behavior of rodents lacking a microbiota—especially social behavior—is remarkably different from that of rodents colonized with bacteria. Conversely, supplementation of animals with certain beneficial live bacteria (e.g., Bifidobacterium and Lactobacillus) can lead to notable improvements in social behavior both in early life and in adulthood. Collectively, these results suggest that microbial signals are important for healthy neurodevelopment and programming of social behaviors in the brain. Although research on the functional and ecological implications of the gut microbiota in natural populations is growing, from an evolutionary perspective it remains unclear why and when relationships between microbes and the social brain arose. We propose that a trans-species analysis may aid in our understanding of human sociability.

ADVANCES

Sociability comprises a complex range of interactive behaviors that can be cooperative, neutral, or antagonistic. Across the animal kingdom, the level of sociability an animal displays is variable; some are highly social (e.g., primates, termites, and honey bees), living within cooperative communities, whereas others have a mostly solitary existence (e.g., bears). Consequently, although studies on germ-free and antibiotic-treated animals have yielded insights into how the microbiota may influence social behaviors, they are perhaps too reductionist to fully appreciate the complex relationship between symbiotic bacteria in the gastrointestinal tract and host sociability when considering a broader zoological perspective. Some social interactions have evolved to facilitate horizontal transmission of microbiota. Observations across both invertebrate and vertebrate species suggest that factors such as diet and immunity generate selection pressures that drive the relationship between microbiota and social behavior. Although microbiota may influence behaviors endogenously through regulation of the gut-brain axis, some animal species may have evolved to use symbiotic bacteria exogenously to mediate communication between members of the same species. Hyenas, for example, produce an odorous paste from their scent glands that contains fermentative bacteria that is suggested to facilitate social cohesion among conspecifics. This complex relationship between animals and microbiota raises the hypothesis that microbes may have influenced the evolution of the social brain and behavior as a means to propagate their own genetic material.

OUTLOOK

Understanding the factors that affect the development and programming of social behaviors across the animal kingdom is important not only in terms of rethinking the evolution of brain physiology and behavior, but also in terms of providing greater insight into disorders of the social brain in humans [including autism spectrum disorders (ASDs), social phobia, and schizophrenia]. Evidence for a link between the microbiota and these conditions is growing, and preclinical and emerging clinical data raise the hypothesis that targeting the microbiota through dietary or live biotherapeutic interventions can improve the associated behavioral symptoms in such neurodevelopmental disorders. Larger clinical trials are required to confirm the efficacy of such interventions before they are recognized as a first-line treatment for neurodevelopmental disorders. Although such connections between gut bacteria and neurodevelopmental disorders are currently an intriguing area of research, any role for the microbiota in the evolution of social behaviors in animals does not supersede other contributing factors. Rather, it adds an additional perspective on how these complex behaviors arose.

The relationship between the microbiota-gut-brain axis and social behavior.

The bidirectional pathway between the gut microbiota and the central nervous system, the microbiota-gut-brain axis, influences various complex aspects of social behavior across the animal kingdom. Some animals have evolved their own unique relationship with their gut microbiota that may assist them in interacting with conspecifics. The relationship between the gut microbiota and social behavior may help to explain social deficits observed in conditions such as autism spectrum disorders (ASDs) and could potentially lead to the development of new therapies for such conditions.

Abstract

Sociability can facilitate mutually beneficial outcomes such as division of labor, cooperative care, and increased immunity, but sociability can also promote negative outcomes, including aggression and coercion. Accumulating evidence suggests that symbiotic microorganisms, specifically the microbiota that reside within the gastrointestinal system, may influence neurodevelopment and programming of social behaviors across diverse animal species. This relationship between host and microbes hints that host-microbiota interactions may have influenced the evolution of social behaviors. Indeed, the gastrointestinal microbiota is used by certain species as a means to facilitate communication among conspecifics. Further understanding of how microbiota influence the brain in nature may be helpful for elucidating the causal mechanisms underlying sociability and for generating new therapeutic strategies for social disorders in humans, such as autism spectrum disorders (ASDs).

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