Effect of one week of stress on emotional reactivity and learning and memory performances in Japanese quail

Abstract

Chronic stress is known to induce long term alterations of emotional behaviours as well as cognitive performances leading thereby to welfare or husbandry problems. These stress-induced consequences are observed following long periods of stress lasting from several weeks to several years. The current study examined whether a shorter period of stress (one week) produced similar impairing effects. Two-week old Japanese quail were either submitted to a series of aversive events over consecutive 8 days, at unpredictable times each day (treated animals) or left undisturbed (controls). Following the treatment period, animals were weighed and basal as well as aversive events-induced levels of plasma corticosterone were quantified. Quail were also tested for emotional reactivity in three tests (the tonic immobility test, the hole-in-the-wall and novel object tests) and for spatial reference memory. Although there was no difference in corticosterone levels between the two groups, the treated animals had lower body weight than controls. Behavioural investigations after the treatment period did not reveal any difference between the groups in the three emotional reactivity tests. In the spatial task, treated quail displayed enhanced behavioural flexibility as revealed by their higher performances during the reversal phase of the task. The alteration of growth suggests that a short period of repetitive exposures to unpredictable aversive events can be perceived by quail as stressful. Such a stress period can improve spatial learning performances in quail supporting the critical role played by the duration of the stress period on cognitive performance.

Introduction

Understanding the relationship between stress and cognitive functioning is an important area of research in pre-clinical studies. It is also relevant in animal research and specifically in farm animal research because stress may disrupt cognitive processes and lead to welfare and husbandry problems. Chronic stress was frequently reported being deleterious for memory performances [8], [22], [31], [34], [42], [47]. Nevertheless, recent studies reported the existence of individual differences in the vulnerability to develop stress-induced learning impairment [46]. In addition, either a lack of effect or even a facilitating effect of stress on spatial memory was previously reported [4], [14]. The most general view to make sense of the discrepancy in the literature is that the relationship between stress intensity–stress hormone levels - and learning and memory performances can take the form of an inverted-U shaped curve [1], [6], [21]. Under moderate or acute stressor, glucocorticoid hormones or other mediator associated with allostasis–a fundamental process that supports adaptation–contribute to maintain and even promote learning and memory capabilities. However, if there are many adverse life events, the secretion of hormone or mediators linked to allostasis can be dysregulated and have damaging effect on learning and memory [35].

Most of the experimental findings investigating learning and memory changes related to chronic stress used long periods of stress [46]. In rodents, a 3- to 5-week period of stress was frequently shown to impair spatial memory in a variety of spatial tasks such as the radial-arm maze [33], the Y-maze [7] and the Morris water maze [45]. Similarly in chicken, 10 weeks of unpredictable light: dark rhythm were shown to disrupt spatial memory [30], [31] and, in seabird chick, a chronically increased circulating level of corticosterone is associated with compromised spatial learning abilities later in life [28].

Studies that specifically investigated the effects of shorter duration of stress periods on cognitive functioning mainly focused on acute stress and only very limited research investigated consequences of intermediate stress duration. No differences in spatial memory are observed in control and stressed rodents following 7 days or 10 days of restrain stress but 13 days of stress were shown to enhance spatial memory [32], [37]. One week of restrain stress was also reported to enhance memory in female rats using the object placement task [3]. Nevertheless, the precise consequences of a sub-chronic period of stress on learning and memory still remain elusive. Moreover, although birds display comparable social and cognitive capacities to mammals [20], the impact of a short period of stress on spatial memory performances in birds, and more specifically in farm birds, still deserve consideration.

In the present study, two-week old quail were divided into control and treated groups. During 8 days, animals from the treated group were submitted to a series of aversive events at unpredictable times each day. To ascertain that the impact of the stress procedure could be investigated on different aspects of behaviour and physiology before sexual maturity, a developmental step that strongly orient the behaviour of the quail, the procedure of stress started when birds were 2 weeks old. A first cohort of animals was used for the measurement, after the treatment, of basal and stress activated corticosterone responses, a typical physiological marker of stress. The second cohort was tested for emotional reactivity and spatial memory performances. Fear reactivity was tested because previous studies reported that individuals frequently exposed to unpredictable environmental stressors tend to have greater response to anxiogenic or acute stressful events [48], [52]. Spatial training was tested to study the consequences of the stress procedure on learning and memory. The aim of this study was thus to provide, in quail, a sub-chronic stress related profile that included both physiological and behavioural consequences of stress.