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mise à jour du
28 août 2003
J Comparative Psychology
2002;116(3):263-269
lexique
Grooming and yawning trace adjustment to unfamiliar environments in laboratory Sprague-Dawley rats (Rattus norvegicus)
Alejandro Moyaho, Jaime Valencia
Benemérita Universidad Autonoma de Puebla
 
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren

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Laboratory rats usually groom and yawn in a stress situation (Dourish & Cooper, 1990). It has been proposed that they groom to reduce arousal (Isaacson & Gispen, 1990) and yawn when the situation inducing the stress is over. Some findings seem to support this observation. For example, rats placed in a novel box groom excessively during the first minutes of exposure. Rats gradually diminish their activity until movement ceases; frequently they yawn and fall asleep. Gulls exposed to a slight, brief disturbance sequentially display orienting, preening, and yawning. The gradual return to normality is marked hy drowsiness and sleepiness (Delius, 1988). Similarly, cats respond to a disturbing stimulus by sniffing, grooming, yawning, lying down, curling up, dozing, and sleeping (Parmeggiani, 1962). Even humans may respond to stress, particularly to situational anxiety, by scratching their head and yawning. Thus, it seems that these behaviors show a gradation of change from arousal to quiescence, which may reflect adjustment to the mild stress that produced them.
 
Findings from other approaches also offer evidence that grooming and yawning and other comfort behaviors are closely related, either motivationally or functionally. For example, the electrical stimulation of forebrain and brainstem structures of gulls produces a sequence of comfort behaviors similar to that caused by an environmental disturbance. The intraventricular irnection of adrenocorticotrophic hormone in cats produces excessive grooming, followed bv stretching and yawning that is accompanied by drowsiness (Gessa, Pisano, Vargiu, Crabai, & Ferrari, 1967).
 
In spite of the extensive work on these behaviors, there are still no studies that have analyzed the temporal relationship between grooming and yawning in situations of mild stress. Such studies would be relevant for understanding how grooming and yawnin contribute to the adjustment to unfamiliar environments. If grooming reduces arousal and yawning signals the termination of the event inducing the stress, then, in situations of moderate stress, rats would prolong grooming and would put off yawning. There are two practical difficulties, however, when testing this prediction. First it is difficult to find a stressor that is stressful, but inoffensive, enou-h. A solution to this problem is to use unpredictable and predictable stimuli, which cause more and less stress, respectively ). Furthermore, these stimuli may be controlled for lasting effects without freezing the animais. Second, most strains of rats tend to yawn infrequently, making it difficult to measure any significant effect of nonpharmacological experiments.
 
Our laboratory at Benernérita Universidad Autônoma de Puebla (Puebla, Mexico) has produced two strains of Sprague-Dawley rats, which were selected for high-yawning (HY) and low-yawning (LY) frequencies (Urbà-Holmgren et al., 1990). The HY strain also grooms more than the LY strain in a novel environment. Therefore, HY rats offer unusual advantages to study the relation between yawning and grooming in response to stress situations.
 
This study investigated the temporal relationship between grooming and yawning in HY rats exposed to mildly stressful situations. The use of brief electric font shocks (which are disturhing rather than painful) allowed us to control the intensity of the stres, event. In addition, we were able to vary the effect of the foot shocks by applying, sequences at fixed intervals (Fis) or randorn intervals (Ris). In the first case, the rats could anticipate the application of the shocks and so adjust accordingly. In the second case, the shocks were unpredictable, and hence, the rats experienced a situation in which it was more difficult to adjust. [...]
 
Discussion :
Although grooming and yawning have been extensively studied, this is the first work that documents their relationship during mild stress. The findings suggest that stress delays the onset of yawning and prolongs grooming. The number of foot shocks does not seem to be a determining factor in such effects, as the rats exposed to FI received twice as many shocks as those subjected to RI, yet yawning diminished more with the latter than with the former. In addition, foot shock number was not a significant predictor of yawning. However, this result should be treated with caution because the data analysis was based on three values of the independent variable (i.e., foot shock number) and because shock number could be confounded with the type of shock regime. The results, though, support the explanation that the degree of predictability of the appearance of the foot shocks determined the way the rats responded. This interpretation accords with the suggestion that the predictability of a stressor or pleasurable stimuli modulates its physiological and behavioral consequences.
 
Because the NS group was in an undisturbed environment (the experimental chamber), it is reasonahle to assume that the rats habituated to it and, hence, that the distribution of groorning and yawning in such a condition reflected that adjustment. Similarly, the decrease in grooming and the increase in yawning in the second session is likely to be a consequence of the adjustment to the chamber. Other studies (Hannigan & Isaacson, 1981; Jolles, Rompa-Barendregt, & Gispen, 1979; Van Erp, Kruk, Melis, & Willekens-Bramer, 1994), however, have not detected changes in groomin- across repeated presentations to stressors (e.g. novelty handling, restraint). This disagreement with the results presented in this study may arise from differences in experimental conditions or from strain-specific responses to novel environments.
 
In any case, if grooming is a direct response to stressful events (Van Erp et al., 1994), then it should decrease after repeated exposures of rats to the same stressor, unless it is a severe stressor. Similarly, if grooming occurs after the end of the stressful event, then an increase should appear later in trials. Our findings, however, show that in every group the highest number of groomings occurred within the first half hour of presentation to the stress situation. This suggests that, at least for the levels of arousal produced in the present experiment, grooming is the initial response to the stressful situation. The findings also suggest that whether foot shocks increase or decrease, total grooming is not, in tact, the issue; what matters is how its distribution changes in response to the stressors. In other words, there seems to be no direct relation between the magnitude of the stressor and the amount of grooming, but rather a dynamic shift in behavior as a function of context.
 
Although foot shocks delivered at Fls did not affect total grooming, they probably delayed its decline and prevented the quik increase of yawning. It, therefore, seems that the foot shocks caused arousal to increase, which later diminished as the foot shocks became predictable and the rats were able to adjust to them as expected. An alternative is that the rats showed an anticipatory fear of encountering an environment that had prevously perturbed them. In such case, fear would be expected to increase with the second exposure and consequently, yawning would be expected to diminish and grooming to increase. The results are not consistent with this possibility rather, they suggest an adjustment to the experimental condition. This is supported by the similarity of the temporal course of the behaviors between NS and FI groups, particularly in the second session. This explanation accords with the idea that the ability to cope with stressors by predicting their appearance may modulate the behavioral and physiological consequences of those stressors. However, this idea is based on studies that frequently used conditioned stimuli to search for associations with physiological or behavioral variables, including grooming. Rarely, however, has the likelihood of the occurrence of an unconditioned stimulus been investigated as a predictive clue to hehavioral responses. Our findings suggest that rats may use such clues to initiate behavioral actions in response to stress.
 
A different scenario was that of RI in which the HY rats could not anticipate the appearance of the foot shocks, as they were randomly presented. The uncertainty so produced might have caused the rats to be anxious, as has been suggested in other studies. Even biochemical disturbances similar to those of depression may appear if rats are subjected to chronic treatment with unpredictable stressors (Katz, Roth, & Carroll, 1981 ). The low rates in grooming and yawning during the first session of RI could be attributable to behavioral inhibition because of the incapacity of the rats to adjust to the situation, as revealed by the lack of groorning habituation. Low levels of grooming associated with decreased motor activity in emotional rats have also been reported as well as immobility with ultrasonic vocalizations in repetitive encounters of rats with resident conspecifics or potenlial predators. Thus, the decrease in yawning and grooming could be the result olf behavioral inhibition.
 
However, in the second session, yawning, and grooming increased; yawning was expected to rise but grooming was not. The fluctuations in grooming and yawning that were sometinies upward and sometimes downward suggest that there was a trade-off between them, as though their courses interfered with each other. A similar trend has been proposed to account for the switching between incompatible behaviors in a model for the crayfish's behavioral commands during stress (Edwards, 1991 ). Such oscillations increase with the size of an inhibitory coefficient, which is a quantitative driving factor of the behavioral commands. leading to higher excitation conditions. Therefore, the fluctuations of yawning and grooming may be the result of excitation caused by the unpredictabilily of foot shocks.
 
How do grooming and yawning help HY rats to adjust to a stress situation? Our findings indicate that the prevalence of grooming or yawning reflects opposing arousal levels: disturbance and quiet. In this study, the relative dominance of one behavior over the other represents shifts in either direction, indicating that HY rats make constant adjustrnents to cope with arousal changes. It is thought that grooming serves for relaxation and yawning for arousal (Baenninger, 1997). Consequently, the action of yawning would be to prevent rats from being relaxed. However, as they and other species eventually fall asleep after exposure to stress situations, it is possible that yawning modulates relaxation so as to prepare for sleeping. The observation that in the NS situation the HY rats yawned frequently before sleeping, with the diminution of yawning and the absence of sleepy rats in the foot shock conditions, supports the role of yawning in modulation of relaxation. In situations of uncertainty, it may be more difficult for the rats to adjust to the context so that they prolong grooming and delay yawning. But, if the disturbing condition continues, then both behaviors tend to co-occur, leading to conflict. The same is probably true in primates (e.g., monkeys. Maccica fascicularis and M. fuscata), including humans, because grooming and yawning have been associated with situational anxiety. If so, then in anxiety disorders, such as obsessive-compulsive disorder, grooming and yawning would tend to co-occur.
 
In summary, this study is the fïrst empirical evidence of' the interaction of grooming and yawning in situations of mild stress. The findings show that although grooming is the forward reaction to diminish arousal, yawning completes the process. Both are mutually inhibitory but complementary behaviors that serve to calm the animal down in arousing conditions. These findings are potentially relevant to an understanding ofhow animals cope with stress-related disorders.
 
Eguibar JR et al Behavioral differences between selectively bred rats: D1 versus D2 receptors in yawning and grooming Pharmacology, Biochemistry and Behavior 2003; 74; 827-832
Eguibar JR et Moyaho A Inhibition of grooming by pilocarpine differs in high-and low yawning sublines of Sprague-Dawley rats. Pharmacoology Biochemistry and Bebavior 1997; 58: 2 317-322
Moyaho A et al Induced grooming transitions and open field behaviour differ in high- and low-yawning sublines of Sprague-Dawley rats Animal Behavior 1995; 50; 61-72
Moyaho A, Valencia J Grooming and yawning trace adjustment to unfamiliar environments in laboratory Sprague-Dawley rats J Comparative Psychology 2002; 116; 3; 263-269
Pandiculation: the comparative phenomenon of systematic stretching AF Fraser