Social fear extinction susceptibility is associated with Microbiota-Gut-Brain axis alterations

•Social fear resiliency and susceptibility are associated with microbiota community composition.•Social fear response is strongly correlated with microbiota variability.•Alterations align with gene sets associated with behaviour, inflammation and immunity, and microbe-host interaction. Social anxiet...

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Published in:	Brain, behavior, and immunity Vol. 120; pp. 315 - 326
Main Authors:	Ritz, Nathaniel L., Bastiaanssen, Thomaz F.S., Cowan, Caitlin S.M., Smith, Linda, Theune, Nigel, Brocka, Marta, Myers, Eibhlís M., Moloney, Rachel D., Moloney, Gerard M., Shkoporov, Andrey N., Draper, Lorraine A., Hill, Colin, Dinan, Timothy G., Slattery, David A., Cryan, John F.
Format:	Journal Article
Language:	English
Published:	Netherlands Elsevier Inc 01-08-2024
Subjects:	Amygdala - metabolism Animals Anxiety - metabolism Brain - metabolism Brain-Gut Axis - physiology Disease Models, Animal Extinction, Psychological - physiology Fear - physiology Gastrointestinal Microbiome - physiology Male Mice Mice, Inbred C57BL Microbiome Phobia, Social - metabolism Phobia, Social - psychology Social anxiety disorder Social Behavior Social fear conditioning Social phobia Social anxiety disorder Social phobia Social fear conditioning Microbiome
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Summary:	•Social fear resiliency and susceptibility are associated with microbiota community composition.•Social fear response is strongly correlated with microbiota variability.•Alterations align with gene sets associated with behaviour, inflammation and immunity, and microbe-host interaction. Social anxiety disorder is a common psychiatric condition that severely affects quality of life of individuals and is a significant societal burden. Although many risk factors for social anxiety exist, it is currently unknown how social fear sensitivity manifests biologically. Furthermore, since some individuals are resilient and others are susceptible to social fear, it is important to interrogate the mechanisms underpinning individual response to social fear situations. The microbiota-gut-brain axis has been associated with social behaviour, has recently been linked with social anxiety disorder, and may serve as a therapeutic target for modulation. Here, we assess the potential of this axis to be linked with social fear extinction processes in a murine model of social anxiety disorder. To this end, we correlated differential social fear responses with microbiota composition, central gene expression, and immune responses. Our data provide evidence that microbiota variability is strongly correlated with alterations in social fear behaviour. Moreover, we identified altered gene candidates by amygdalar transcriptomics that are linked with social fear sensitivity. These include genes associated with social behaviour (Armcx1, Fam69b, Kcnj9, Maoa, Serinc5, Slc6a17, Spata2, and Syngr1), inflammation and immunity (Cars, Ckmt1, Klf5, Maoa, Map3k12, Pex5, Serinc5, Sidt1, Spata2), and microbe-host interaction (Klf5, Map3k12, Serinc5, Sidt1). Together, these data provide further evidence for a role of the microbiota-gut-brain axis in social fear responses.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	0889-1591 1090-2139 1090-2139
DOI:	10.1016/j.bbi.2024.06.009