Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats
Psychoneuroendocrinology. 2014-04-01; 42: 207-217
DOI: 10.1016/j.psyneuen.2014.01.014
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Crumeyrolle-Arias M(1), Jaglin M(2), Bruneau A(2), Vancassel S(3), Cardona A(4), Daugé V(5), Naudon L(5), Rabot S(6).
Author information:
(1)INSERM, UMRS952 Physiopathologie des Maladies du Système Nerveux Central,
F-75005 Paris, France; CNRS, UMR7224 Physiopathologie des Maladies du Système
Nerveux Central, F-75005 Paris, France; UPMC, Physiopathologie des Maladies du
Système Nerveux Central, F-75005 Paris, France.
(2)INRA, UMR1319 Micalis, F-78350 Jouy-en-Josas, France; AgroParisTech, Micalis,
F-78350 Jouy-en-Josas, France.
(3)INRA, UR0909 Nurelice, Jouy-en-Josas, France.
(4)Institut Pasteur, Plateforme Imagerie Dynamique, Paris, France.
(5)INSERM, UMRS952 Physiopathologie des Maladies du Système Nerveux Central,
F-75005 Paris, France; CNRS, UMR7224 Physiopathologie des Maladies du Système
Nerveux Central, F-75005 Paris, France; UPMC, Physiopathologie des Maladies du
Système Nerveux Central, F-75005 Paris, France; CNRS, Micalis, F-78350
Jouy-en-Josas, France.
(6)INRA, UMR1319 Micalis, F-78350 Jouy-en-Josas, France; AgroParisTech, Micalis,
F-78350 Jouy-en-Josas, France. Electronic address: .
BACKGROUND AND AIMS: Establishment of the gut microbiota is one of the most
important events in early life and emerging evidence indicates that the gut
microbiota influences several aspects of brain functioning, including reactivity
to stress. To better understand how the gut microbiota contributes to a
vulnerability to the stress-related psychiatric disorders, we investigated the
relationship between the gut microbiota, anxiety-like behavior and HPA axis
activity in stress-sensitive rodents. We also analyzed the monoamine
neurotransmitters in the brain upper structures involved in the regulation of
stress and anxiety.
METHODS: Germfree (GF) and specific pathogen free (SPF) F344 male rats were
first subjected to neurological tests to rule out sensorimotor impairments as
confounding factors. Then, we examined the behavior responses of rats to social
interaction and open-field tests. Serum corticosterone concentrations, CRF mRNA
expression levels in the hypothalamus, glucocorticoid receptor (GR) mRNA
expression levels in the hippocampus, and monoamine concentrations in the
frontal cortex, hippocampus and striatum were compared in rats that were either
exposed to the open-field stress or not.
RESULTS: GF rats spent less time sniffing an unknown partner than SPF rats in
the social interaction test, and displayed a lower number of visits to the
aversive central area, and an increase in latency time, time spent in the
corners and number of defecations in the open-field test. In response to the
open-field stress, serum corticosterone concentrations were 2.8-fold higher in
GF than in SPF rats. Compared to that of SPF rats, GF rats showed elevated CRF
mRNA expression in the hypothalamus and reduced GR mRNA expression in the
hippocampus. GF rats also had a lower dopaminergic turnover rate in the frontal
cortex, hippocampus and striatum than SPF rats.
CONCLUSIONS: In stress-sensitive F344 rats, absence of the gut microbiota
exacerbates the neuroendocrine and behavioral responses to acute stress and the
results coexist with alterations of the dopaminergic turnover rate in brain
upper structures that are known to regulate reactivity to stress and
anxiety-like behavior.
Copyright © 2014 Elsevier Ltd. All rights reserved.