The influence of a probiotic supplementation on memory in quail suggests a role of gut microbiota on cognitive abilities in birds

Parois, Séverine; Calandreau, Ludovic; Kraïmi, Narjis; Gabriel, Irène; Leterrier, Christine

doi:10.1016/j.bbr.2017.05.022

Cited by 42 publications

(34 citation statements)

References 42 publications

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“…Azeem (2013) showed that the administration of the probiotic Bacillus amyloliquefaciens helped to reduce distress calls and agonistic behaviour in turkeys. More recently, a decrease in emotional reactivity in a tonic immobility test and memory improvement have been described by Parois et al (2017) following continuous supplementation with the probiotic Pediococcus acidilactici in Japanese quails.…”

Section: Introductionmentioning

confidence: 99%

Effects of a gut microbiota transfer on emotional reactivity in Japanese quails (Coturnix japonica)

Kraïmi¹,

Calandreau²,

Zemb

et al. 2019

Journal of Experimental Biology

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The interaction between the gut microbiota (GM) and the brain has led to the concept of the microbiota-gut-brain axis but data for birds remain scarce. We tested the hypothesis that colonization of germfree chicks from a quail line selected for a high emotional reactivity (E+) with GM from a line with low emotional reactivity (E−) would reduce their emotional behaviour in comparison with germ-free chicks from an E+ line colonized with GM from the same E+ line. The GM composition analysis of both groups revealed a shift in terms of microbial diversity and richness between day 21 and day 35 and the GM of the two groups of quails were closer to each other at day 35 than at day 21 at a phylum level. Quails that received GM from the E− line expressed a lower emotional reactivity than quails colonized by GM from the E+ line in tonic immobility and novel environment tests carried out during the second week of age. This result was reversed in a second tonic immobility test and an open-field run 2 weeks later. These behavioural and GM modifications over time could be the consequence of the resilience of the GM to recover the equilibrium present in the E+ host, which is in part driven by the host genotype. This study shows for the first time that a GM transfer can influence emotional reactivity in Japanese quails, supporting the existence of a microbiota-gut-brain axis in this species of bird.

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Section: Introductionmentioning

confidence: 99%

Effects of a gut microbiota transfer on emotional reactivity in Japanese quails (Coturnix japonica)

Kraïmi¹,

Calandreau²,

Zemb

et al. 2019

Journal of Experimental Biology

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“…In addition, the administration of the probiotic Bacillus amyloliquefaciens helped to reduce agonistic behavior and distress calls in turkeys (Azeem, 2013 ). More recently, it has been shown that continuous supplementation from hatching with a probiotic ( Pediococcus acidilactici) in Japanese quails caused a decrease in emotional reactivity in the tonic immobility test and improved memory (Parois et al, 2017 ). These results suggest that the gut microbiota is able to modify emotional behavior in poultry birds, as previously observed in rodents.…”

Section: Introductionmentioning

confidence: 99%

“…Therefore, the aim of the present study was to determine the effect of the absence of gut microbiota on emotional reactivity in birds by comparing germ-free to colonized quails, an experiment never before conducted in birds. The Japanese quail ( Coturnix japonica ), a precocial bird, was chosen as a model in this study due to its capacities to live without its mother in early life, thus limiting the influence of maternal microbiota, and also because the effects of a probiotic on emotional behavior of this bird have already been demonstrated in previous work from our laboratory (Parois et al, 2017 ). It was recently reported that the host's genetic could influence the effects of the gut microbiota on behavior (Crumeyrolle-Arias et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

Absence of Gut Microbiota Reduces Emotional Reactivity in Japanese Quails (Coturnix japonica)

et al. 2018

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Background: Recent studies have demonstrated an effect of the gut microbiota on brain development and behavior leading to the concept of the microbiota-gut-brain axis. However, its effect on behavior in birds is unknown. The aim of the present study was to determine the effect of the absence of gut microbiota on emotional reactivity in birds by comparing germ-free (GF) quails to those colonized (COL) with gut microbiota.Material and Methods: From hatching, the quails of both groups GF (n = 36) and COL (n = 36) were reared in sterile isolators. The COL quails were colonized at day 2 by introducing a pool of droppings from conventional adult females into the drinking water and feed. The quails were weighed individually on day 2, 6, and 14. From day 8, emotional reactivity was assessed in each group in the isolators through several behavioral tests.Results: GF quails showed a considerable decrease in emotional reactivity demonstrated by spending less time in tonic immobility during the tonic immobility test (242 s ± 31 vs. 331 s ± 32, p ≤ 0.05), traveling a shorter distance (3,897 cm ± 242 vs. 4,827 cm ± 278, p ≤ 0.05) at a lower velocity (6.55 cm/s ± 0.4 vs. 8.1 cm/s ± 0.5, p ≤ 0.05) during the social separation test and spending more time near an object at the beginning of the novel object test (33.7 s ± 6.4 vs. 18.5 s ± 4.1, p ≤ 0.05). No difference in growth was found between the 2 groups.Conclusion: For the first time, this study demonstrates that the absence of gut microbiota reduces emotional reactivity in Japanese quails in situations of fear and social perturbation without influence on growth.

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“…Moreover, germ-free mice colonized with microbiota from another mouse strain exhibit behavioural profiles of the donor strain 13 . The gut microbiota seems to have similar effects in poultry, where altering microbiota composition affects fearfulness, memory, and serotonergic and immune systems [14][15][16] . Moreover, microbiota transplantation to germ-free quails has resulted in recipients adopting the fearful behaviour of donors early in life; however, this effect reversed later Microbial groups for which the variation in relative abundance in the data is explained for at least 95% by the axes are represented as vectors.…”

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Early-life microbiota transplantation affects behavioural responses, serotonin and immune characteristics in chicken lines divergently selected on feather pecking

Eijk

Rodenburg

Vries

et al. 2020

Sci Rep

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in life 17. These findings suggest that the gut microbiota influences behavioural and physiological characteristics in poultry and could therefore influence a bird's ability to cope with environmental and social challenges, such as those encountered in animal production systems. Excessive damaging behaviours are indicative of an animal's inability to cope with a restrictive environment and are frequently seen in production animals. Feather pecking (FP) in chickens is one such damaging behaviour, which involves hens pecking and pulling at feathers of conspecifics, thereby reducing animal welfare and productivity 18. Feather pecking is multifactorial and has been linked to numerous behavioural characteristics, such as fearfulness, stress and activity, as well as physiological characteristics, such as serotonergic, dopaminergic and immune systems 19-21. Since behavioural and physiological systems that are related to FP are also affected by the gut microbiota, microbiota might play a role in the development of FP. Indeed, lines selected for high FP (HFP) and low FP (LFP) differ in behavioural responses, stress response, activity, central serotonergic and dopaminergic activity, peripheral serotonin, innate and adaptive immune characteristics 22-28. Moreover, the HFP and LFP lines differ in intestinal microbial metabolites and microbiota composition determined from caecal droppings and intestinal luminal content 29-31. These findings point to a relationship between the gut microbiota and FP, however, it is unknown whether the gut microbiota influences the development of FP. Therefore, this study aims to identify the effects of early-life microbiota transplantation on FP and behavioural and physiological characteristics related to FP in lines divergently selected for FP (HFP and LFP lines). We further identify the effects of microbiota transplantation on microbiota composition. We hypothesize that microbiota transplantation results in recipients adopting a similar behavioural profile as that seen in the donor line. For example, LFP birds receiving HFP microbiota show more FP and more active behavioural responses compared to LFP birds receiving LFP microbiota or control treatment. Results High and low feather pecking transplantation pools had distinct microbiota composition. Gut microbiota was collected from adult chickens of the HFP and LFP lines that were shown to differ in microbiota composition 31. Transplantation pools were made per line and could be distinguished from each other in terms of microbiota composition using a principal component analysis (PCA) (Fig. 1A). The orders of Clostridiales and Lactobacillales had the highest relative abundance in both pools. The HFP pool had a higher relative abundance of

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The influence of a probiotic supplementation on memory in quail suggests a role of gut microbiota on cognitive abilities in birds

Cited by 42 publications

References 42 publications

Effects of a gut microbiota transfer on emotional reactivity in Japanese quails (Coturnix japonica)

Effects of a gut microbiota transfer on emotional reactivity in Japanese quails (Coturnix japonica)

Absence of Gut Microbiota Reduces Emotional Reactivity in Japanese Quails (Coturnix japonica)

Early-life microbiota transplantation affects behavioural responses, serotonin and immune characteristics in chicken lines divergently selected on feather pecking

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