Japanese Quail’s Genetic Background Modulates Effects of Chronic Stress on Emotional Reactivity but Not Spatial Learning

et al. (2012) Japanese Quail's Genetic Background Modulates Effects of Chronic Stress on Emotional Reactivity but Not Spatial Learning. PLoS ONE 7(10): e47475. doi:10.1371/journal.pone.0047475 Japanese Quail's Genetic Background Modulates Effects of Chronic Stress on Emotional Reactivity but Not Spatial Learning Agathe Laurence 0 Ce cilia Houdelier 0 Christophe Petton 0 Ludovic Calandreau 0 Ce cile Arnould 0 Ange lique Favreau-Peigne 0 Christine Leterrier 0 Alain Boissy 0 Marie-Annick Richard-Yris 0 Sophie Lumineau 0 Claudia Mettke-Hofmann, Liverpool John Moores University, United Kingdom 0 1 Ethos UMR 6552, Universite de Rennes 1, CNRS, Rennes, France, 2 UMR 85 Physiologie de la Reproduction et des Comportements, INRA, CNRS, Universite de Tours, Nouzilly, France, 3 Unite de Recherche sur les Herbivores, INRA, St Gene`s Champanelle, France, 4 UMR791 Mod e lisation syste mique applique e aux ruminants, INRA , Paris , France Chronic stress is known to enhance mammals' emotional reactivity and alters several of their cognitive functions, especially spatial learning. Few studies have investigated such effects in birds. We investigated the impact of a two-week stress on Japanese quail's emotional reactivity and spatial learning. Quail is an avian model widely used in laboratory studies and for extrapolation of data to other poultry species. As sensitivity to chronic stress can be modulated by intrinsic factors, we tested juvenile female Japanese quail from three lines, two of them divergently selected on tonic immobility duration, an indicator of general fearfulness. The different emotional reactivity levels of quail belonging to these lines can be revealed by a large variety of tests. Half of the birds were submitted to repeated unpredictable aversive events for two weeks, whereas the other half were left undisturbed. After this procedure, two tests (open field and emergence tests) evaluated the emotional reactivity of treated and control quails. They were then trained in a T-maze for seven days and their spatial learning was tested. The chronic stress protocol had an impact on resting, preening and foraging in the home cage. As predicted, the emotional reactivity of treated quails, especially those selected for long tonic immobility duration, was higher. Our spatial learning data showed that the treatment enhanced acquisition but not memorization. However, intrinsic fearfulness did not seem to interact with the treatment in this test. According to an inverted U-shaped relationship between stress and cognition, chronic stress can improve the adaptability of birds to a stressful environment. We discussed the mechanisms possibly implied in the increase of emotional reactivity and spatial abilities. - Funding: This work was supported by the French National Research Agency (ANR), project Emofarm http://www.agence-nationale-recherche.fr/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Whether natural or experimental, chronic stress has numerous influences on the physiology and behaviour in various species [1,2]. In experimental conditions, chronic stress is defined as a prolonged period of stress during which an individual is exposed to continuous or repeated psychological stressor(s) without habituation, by unpredictable administration of different types of intermittent mild stressors [3]. Chronic stress can affect growth, hypothalamus-pituitary-adrenal (HPA) axis response and emotional reactivity, and can induce several brain and cognitive alterations [46]. However, analysis of the numerous studies in this field shows that chronic stress effects are protocol dependent, especially in regard to the intensity and the duration of the stressors used [79]. In mammal studies, chronic stress procedures aim to induce long-term and marked effects such as anhedonia used as models in the etiology of human depression [1013]. By contrast, chronic stress effects on the behaviours of other taxa are scarce (amphibians: [14], fish: [15,16]) and then procedures seem to be less rigorous than those used for rodents. Whereas reports show that chronic stress procedures can influence birds physiological parameters (Starlings (Sturnus vulgaris: [3,1719], Japanese quail (Coturnix c. Japonica): [20]) very few studies have investigated behavioural changes [21,22]. Other avian studies using artificially induced postnatal stress (e.g. corticosterone feeding or injections) evidenced HPA axis modifications and enhanced emotional reactivity or impaired cognitive performance [2325]. However, previous studies on starlings, zebra finches (Taeniopygia guttata) and Japanese quail report a decrease of basal corticosterone levels after exposure to unpredictable and repetitive mild stressors [3,17,22] and chronically stressed birds cognitive abilities vary between studies [21,26]. Thus, regardless of the species studied, these results raised the possibility of an inverted U-shaped relationship between stress intensity and cognitive functions [27]. Another source of variability of the effects of chronic stress procedures could be inter-individual variability of the sensitivity to chronic stress procedures [2831]. Indeed, the more emotive an individual is the more sensitive to environmental stressors it might be. Japanese quail, a terrestrial bird used in the laboratory and poultry stock breeding have been selected for either low or high emotional reactivity [32]. In fact, tonic immobility (TI), a reflexive antipredator response correlated to general fearfulness, varies greatly in duration [33]. Several traits of the fear responses of Japanese quail selected for either short or long TI durations (respectively STI and LTI) diverge [3438]. These two selected lines of Japanese quail were used in this study to test the impact of intrinsic emotional reactivity on the sensitivity to a two-week chronic stress procedure. As birds chronic stress has been poorly studied, we first assessed how spontaneous behaviour in their home cage was affected by our procedure and estimated its possible modulation by intrinsic fearfulness. Then, two major aspects of chronic stress effects were investigated: emotional reactivity in a novel environment (open or closed) and spatial learning. Chronic stress increases emotional reactivity and anxiety [13]. Moreover, fearful individuals are more sensitive to changes in their environment [39]. Thus, we hypothesized that sensitivity to chronic stress procedure depends on intrinsic fearfulness, then LTI treated quail should be the most affected by a novel environment and that STI quail (the least fearful) would be less affected by our procedure than LTI quail (the most fearful). Quail which are the most sensitive about chronic stress should be more reactive in novel environment, depending on the situation. Previous studies report t (...truncated)