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mise à jour du 15 mai 2003
Animal Behavior
1995;50:61-72
lexique
 
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Induced grooming transitions and open field behaviour differ in high- and low-yawning sublines of Sprague-Dawley rats
A. Moyaho, JR Eguibar, JL Diaz
Centro de Ciencias Fisiologicas , Instituto de Ciencias
Universidad Autonoma de Puebla, Mexico
 
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren

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In the last two decades the study of grooming has become the subject of extensive research, primarily because of its usefulness in modelling hierarchical motor control and because grooming is structurally organized in a variety of movements that can be analysed for identifying rules that govern behavioural sequencing. This approach may provide insights into the way the central nervous system controls chains of rhythmical movements. In addition, grooming can be produced easily by either novel environments or water immersion, which makes it possible to record many bouts of grooming for long periods.
 
A variety of evidence suggests that grooming in a number of vertebrate and invertebrate species is centrally organized, and that rodents groom in a cephalo-caudal progression which resembles the order in which grooming actions appear in developing animals. The biological significance of grooming is still not clear, although studies indicate that it represents a de-arousal mechanism serving homeostasis, and is generally considered to be a motor pattern with adaptive functions beyond the simple care of fur.
 
Most ethological studies regarding grooming have been concerned with the analysis of its temporal patterning, mainly by the use of two methods: serial dependence and hierarchical analysis models, the latter appear to explain the patterning of grooming better than the former. Detailed studies in mammals, insects, and birds have led to the suggestion that grooming is hierarchically organized, that grooming movements cluster into anterior and posterior groups according to body regions, and that the transition between grooming acts appears to follow specific rules such as perseverance and reciprocity.
 
These studies reveal that many features of grooming are common to several species, and that grooming appeared very early in the evolution of animals. However, some quantitative aspects of grooming may vary from one species to another, even within species. For example, Fentress (1968) found that duration of grooming differed between two species of voles after exposure to an overhead moving object, suggesting varying "optimal arousal" levels amongst species. Moreover, face grooming frequency was distinct between two strains of mice. Berridge (1990) found a similarity in the patterning of grooming among several species of rodents. The small differences in duration of single elements were attributed to phenotypical (allometric control) or genotypical (phylogenetic relatedness) aspects. There is also evidence that aspects, such as grooming bout length, are distinct in species of American squirrels, and that these differences may be attributed to ecological factors, which have rarely been considered in grooming analysis.
 
Grooming and other types of behaviour, particularly yawning, are elicited by intracerebroventricularly injected neuropeptides suggesting that both behaviour patterns share some of the neural mechanisms involved in their generation. Yawning, like grooming. is a current behaviour in many species and has gained the attention of many investigators. Contrary to grooming, yawning seems to be an arousal mechanism that serves to preserve wakefulness. It has been suggested, however, that yawning and preening, which is the avian equivalent of grooming, are comfort patterns that are related to each other, either motivationally or functionally. In humans, yawning has been considered as a stereotyped action pattern associated with sleeping and waking. Little is known, however, of what function yawning may serve or what environmental circumstances modulate its rate. There is no further information about the relationship between grooming and yawning, probably because in contrast with grooming, yawning can not be elicited by environ mental manipulations, but only by the adrninistration of drugs. This makes it difficult to carry out experiments to assess which environmental conditions modulate yawning rates and its relation to other types of behaviour such as grooming.
 
In this paper we present a comparative analysis of grooming in two sublines of Sprague-Dawley rats selectively bred for high- (HY) and lowyawning (LY) frequency. The main advantage of using these two strains of rats is that it allows us to assess the effect that yawning has on the structure of behaviour patterns that are sensitive to environmental manipulations. Our study focuses mainly on quantitative aspects of grooming structure, and because in preliminary observations we detected that HY rats were more active than LY rats, we also included open field tests, which are commonly used for measuring behaviour believed to be involved in emotional reactivity. Besides ease of performance, some of the open field measured behaviour patterns are sensitive to genetic and experimental manipulations which reinforce their ecological validity.[...]
 
Discussion:
High- and low-yawning Sprague-Dawley rats differ in many open field and induced-grooming behaviour patterns. This finding is consistent with inbred selection studies revealing that genetic influences are ubiquitous for animal behaviour. The results of the open field test show that HY rats are more active than LY rats, indicating that they are less emotionally reactive than the latter. This suggestion is supported by the fact that both groups of rats varied with respect to ambulation, and to a lesser extent, defecation, the two most reliable parameters in open field tests, and in accordance to current open field behaviour interpretations. We conclude that the inbred selection carried out on HY and LY rats appears to parallel a low and high level, respectively, of emotional reactivity, and from this we can predict the existence of an inverse correlation between yawning frequency and emotional reactivity. With the present results we cannot confirm the above-mentioned hypothesis, in part because we did not record yawns and in part because the open field test lasted only 15 min, which is a short period for yawning behaviour to appear. A corroboration of this is the suggestion that yawning might signal the termination of a stressful situation instead of being present throughout it. Although we did not find any significant difference in open field grooming behaviour, it is possible that the continuous sampling method we used, was not appropriate to detect differences in grooming between the two groups of rats, or that the difference between the groups was in time engaged in behaviour other than grooming. These results agree with the suggestion that in open field tests, grooming does not seem to be related to indexes of emotional reactivity.
 
The analysis of water immersion-induced grooming revealed that LY rats include more movements than HY rats in their grooming sequences. This overall difference indicates that LY rats perform longer sequences of grooming, and that they also spend more time in each sequence of grooming. Of course, it might be that both HY and LY rats spend the same time in each sequence of grooming, but with LY rats performing the task more quickly than HY rats. Our initial suggestion, however, is supported by the analysis of grooming transitions, which indicated that LY rats execute more transitions between grooming acts. Our results partially parallel those of other studies suggesting quantitative differences in grooming behaviour between different strains of mice or rats. Despite the quantitative differences in grooming between HY and LY rats, both groups of rats groom according to a cephalocaudal progression, as bas been found by other authors. It should be noted that this progression also implies that animals use more acts for grooming their facial than caudal part. Therefore. there is a cephalo-caudal progression not only of order but also of number of grooming movements.
 
Correspondence analysis revealed that grooming acts, in both HY and LY rats, are hierarchically organized. This complex structure instead of a serial dependence of grooming acts has been found by other authors and appears to be a common feature in many species. The functional implications of this structure have not been clarified, although it might be that in terms of costs and benefits it is more advantageous for an animal to groom by recruiting several movements and directing them to specific areas than to groom by executing a chain of single movements. which would require a repetitive 'coming and going' mechanism investing more time and losing efficiency of grooming. HY and LY rats also groom according to precise rules: the transitions between grooming acts depend on anatomical proximity, whereas their clustering which is the main characteristic of a hierarchical organization. requires not onl~ the recruitnient of a number of acts but also certain degree of transitional reciprocity between them. This implies thai clustering of grooming acts does not necessarily have to be related to anatomical regions as has been suggested. For instance. our results indicate that elustering of facial acts include mouth-sides, which is a movement directed to the trunk, anatomically far and distinct from the facial area.
The present study also detected a quantitative and organizational 'polarization' of grooming movements between HY and LY rats. LY rats perform more clustered facial acts. whereas HY rats engaged in more clustered caudal acts. This distinct 'syntax' of grooming indicates a lunetional and neurophysiological différence between both groups of rats. If this suggestion is correct it would indicate that the central nervous system commands grooming movements in a distinct way for HY and LY rats. maybe by emphasizing the action of certain neural structures and inhibiting others. Also it might be that two neural subsystems exist for controlling facial and caudal grooming.
 
For instance, patterns of locomotion based on rhythmic movements have been studied in a number of lower vertebrate groups, revealing an alternation of muscular activity between head and tail portions that might be determined centrally. The findings relating to the polarization of grooming behaviour between HY and LY rats opens new possibilities for studying the underlying neural mechanisms that control grooming organization. Whether this polarization is related to a functional significance is not yet clear, but it is likely that differences in grooming between HY and LY rats are associated with other behavioural traits. Concerning this, results in our laboratory indicate that spontaneous and pharmacologically-induced yawning in HY rats is positively correlated with penile erections. Thus. the 'excessive' caudal grooming of the HY subline may be related to sexual function, a conclusion reached by Moore & Rogers (1984). showing that self-grooming in young male rats contributes to the maturation of genitalia. Similarly, the fact that LY rats have a higher number of body shakes suggests that this behaviour has an adaptive function. By performing it repeatedly, animals rid their fur of a great quantity of water. Accordingly, we predict that LY rats would dry their body fur in less time. which is consistent with the finding that they engage in less caudal grooming. Therefore, LY rats would direct most of their grooming behaviour towards facial instead of caudal areas. This suggestion is consistent with the results of correspondence analysis of LY rats that indicate that body shakes and pauses are closely related, with the latter serving as transitional elements between facial and caudal grooming.
 
The hierarchical organization of grooming of HY and LY rats also agrees with predictions derived from the decision-making hypothesis of Dawkins & Dawkins (1973). HY and LY rats 'decision points' different Dawkins 1973) mainly at the transition between facial and caudal grooming. Alternatives of drying distinct parts of the body may be partially determined at the level of these decisions points; mouth abdomen for HY and pauses for LY rats. Although the structure of grooming behaviour of HY and LY rats appears to have a strong influence from the central nervous system. it is also clear that external factors are involved in their initiation and termination. In our experiments, we wet the rats, eliciting the initiation of a natural sequencing of groommg, which rats execute to dry their fur quickly and efficiently because body temperature may drop. Efficient drying requires a continuous flow of information between the peripheral and central nervous system. But once such goal-directed behaviour bas been displayed, feedback mechanisms should either switch to other areas of activity or stop ongoing activity. We would expect that with warm water, rats also exhibit a natural sequence of grooming, but complete their drying in less time. It remains, however, to be discovered which parts of the central nervous system command these decisions. Recently, Berridge & Wishaw (1992) showed that neuronal structures like the striatum are involved in the control of the serial order of grooming. Therefore, HY and LY rats may have endogenous modifications in the basal ganglia imposed by selection, and that may explain some of the differences in grooming sequences that we have found. Although grooming appears to depend to a large extent on the influence of the central nervous system, evidence suggests that it is also under the control of postural facilitation, feedback mechanisms, allometric control, and as our results suggest, strain-specific functional and neurophysiological aspects.
 
A crucial question is whether yawning, grooming and emotional behaviour are related. Our results show that along with a high or low frequency of yawning, there are other traits that altogther separate HY and LY rats. A possibility is that all these differences are only side-products of the inbred selection and that the behavioural heterogeneity we found between both groups of animals is a mechanism evolved against homozygocity which might be disadvantageous for a population. In this context, small genetic changes may cause behavioural differences of great importance in the speciation of animals. A second alternative is that these differences represent the separation of behavioural systems, a concept that makes it possible to explain that a number of behaviour patterns are related either functionally or motivationally. The behavioural system we detected resembles that reported by Delius (1988). When gulls were disturbed by an external stimulus, they exhibited a sequence of behaviour patterns that included preening, yawning and sleeping, suggesting that when there is a change in the ongoing arousal level, animals display a set of behaviour patterns leading to restore the previous state of arousal. In mammals, yawning has been associated with transitions between waking and sleeping, and after exposure to stressful situations whereas grooming is believed to be involved in decreasing an enhanced arousal. Therefore, both types of behaviour seem to be associated with changes of ongoing arousal. It might be that the selection carried out on HY and LY rats also separated those types of behaviour that are associated with specifical thresholds of arousal. Because of the obvious advantages of having a high yawning strain, the majority of the studies in our laboratory have focused on them, and preliminary results have revealed that HY rats in a novel environment, other than an open field cage, show increased grooming followed by yawning and sleeping (unpublished data), confirming the observation of Delius (1988). Further results are necessary to confirrn these hypotheses, but we believe that with this initial approach, new insights are gained about yawning, grooming and their relationship.
 
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
Eguibar JR et al Behavioral differences between selectively bred rats: D1 versus D2 receptors in yawning and grooming Pharmacology, Biochemistry and Behavior 2003; 74; 827Ð832
Moyaho A et al Induced grooming transitions and open field behaviour differ in high and low-yavning sublines of Sprague-Dawley rats. Anim Behav 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
Moyaho a et al. Genetic and littermate influences on yawning in two selectively bred strains of rats Dev Psychobiol 2008 in press
Urba-Holmgren R, Trucios N, Holmgren B, Eguibar JR, Gavito A, Cruz G, Santos A Genotypic dependency of spontaneous yawning frequency in the rat Behav Brain Res 1990 Oct 30;40(1):29-35
Urba-Holmgren R, Santos A, Holmgren B, Eguibar JR Two inbred rat sublines that differ in spontaneous yawning behavior also differ in their responses to cholinergic and dopaminergic drugs Behav Brain Res 1993 Sep 30;56(2):155-9
Urba-Holmgren R, Holmgren B, Rodriguez R, Gonzalez RM Serotonergic modulation of yawning Pharmacol Biochem Behav 1979 Sep;11(3):371-2
Urba-Holmgren R, Gonzalez RM, Holmgren B Is yawning a cholinergic response? Nature 1977 May 19 267 (5608): 261-2 et commentaires Cholinergic link in yawning A Cowan Nature 12/01/78 271 p187-188
Urba-Holmgren R, Holmgren B, Leon BA, Ugarte A Age-dependent changes in serotonergic modulation of yawning in the rat. Pharmacol Biochem Behav 1992 Oct;43(2):483-6
Argiolas A Yawning and penile erection: central dopamine-oxytocin-adrenocorticotropin connection Ann N Y Acad Sci1988;525:330-7