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11 novembre 2002
Pharmacoology Biochemistry and Bebavior 1997;58; 2; 317-322
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Inhibition of grooming by pilocarpine differs in high-and low yawning sublines of Sprague-Dawley rats
Eguibar JR, Moyaho A
Instituto de Fisiologa, Universidad Autonoma de Puebla Mexico
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren


Grooming occurrence in several species of animals, as a result of environmental manipulations, has generated an increasing interest in the study of this behavior, and many authors have suggested that grooming serves a variety of adaplive functions. In rodents, grooming can be elicited by either exposure to a novel environment, including handling and transportation of the animal to an observation room, or immersion in water, which allows the recording of repetitive and natural sequences of grooming for long periods. Grooming and other behaviors, particularly yawning, which is less susceptible to modification by environmental manipulations, are increased by the i.c.v. administration of ACTH, a-MSH and related neuropeptides suggesting that these behaviors might share some of their underlying neurochemical mechanisms.

The fact that the prior administration of naloxone, a nonselective opioid antagonist, and other neurotransmitter substances prevent environmental or pharmacological induced grooming, suggests a complex interaction among several neural systems. For instance, the muscarinic receptor antagonists atropine and scopolamine can specifically antagonized, in a dose-dependent manner, ACTH-induced grooming. Similarly, a previous injection of atropine into the ventral tegmental area inhibits grooining induced by the i.c.v. adininistration of a-MSH. A prior injection of muscarinic antagonists also suppressed the effect of bombesin-stimulated grooming. Spontaneous and drug-induced yawning have also been related to a cholinergic influence, especially to an excitatory action by the administration of cholinomimetic substances.

These findings indicate that grooming and yawning are under the influence of the muscarinic cholinergic system. However, there are no studies that reveal a direct relation between grooming frequency and cholinergic drugs, as there are for yawning. This is because most pharmacological studies have focused ou the ability of cholinergic antagonists to reverse grooming induced by neuropeptides. In addition, most studies have been carried out either on grooming or yawning, but rarely considering the relationship between both behaviors, probably because in contrast to grooming, yawning occurs witlh a low spontaneous frequency which restricts its analysis to pharmacological manipulations.

ln our laboratory we have developed two sublines of Sprague-Dawley rats, selectively bred for high-(HY) and lowyawning (LY) frequency, and it bas been shown that they differ in their responses to cholinergic and dopaminergic drugs as well as in emotional reactivity and hierarchical composition of grooming elements. In this study we tested whether novelty and water immersion-induced grooming frequency differ between HY and LY rats in a way that it parallels the difference in yawning between both groups of rats. We also examined whether pilocarpine increases grooming as it docs with yawning. The results indicate a genotypic variation between HY and LY rats that supports the first hypothesis of the study, but not the latter. [...]

Discussion : The present results show that HY rats groom more than LY when they are exposed to a novel environment or after immersion in water. Thee latter produces a higher amount of grooming than the novel testing condition, which is in accordance with other experiments. The difference in grooming between HY and LY rats, which parallels that of spontaneous yawning frequency shown by both sublines, indicates a positive correlation between yawning and grooming and suggests that the selection for yawning frequency also affected grooming.
Previous results showed that HY and LY rats also differ in open field activity and the hierarchical organization of grooming elements, which supports the findings of this report and demonstrates that the differences between both strains of rats go beyond yawning frequency.
Whether these behavioral differences are a direct or secondary consequence of the inbred selection is still not clear, although it is consistent with other inbred selection studies that have revealed that genetic influences are ubiquitous for animal behavior. It is possible that yawning and grooming have a motivational or functional relationship, other than that concerning their pharmacological induction. It has previously been suggested that these behaviors are after responses to stressful stimuli or circumstances. If this were the case, il would follow that HY rats are more sensitive to stressful circumstances, a conclusion partially supported by preliminary results, and to the pituitary-adrenal system, which is activated as an animal's reaction to exposure to novel stimuli.
Indeed, it has been reported that the central release of ACTH can be involved in the increased grooming observed in a novel environment, and probably in that after immersion in water. The finding that HY animals maintain a high level of grooming in a novel condition and after immersion in water, supports the idea that both kinds of grooming response insight be similar with respect to the neurochemical mechanisms of their generation. Stressors such as fur moistening may differ from exposure to a novel condition and from immersion in water, which not only disturbs the fur of the animal but also makes it too dry. Therefore, drying after water immersion seems to overcorne grooming caused by solely moistening the fur. It is interesting that the difference in novelty-induced grooming between HY and LY rats is restricted to face washing and scratching, which have been considered as components of two sub-branches in the grooming system, suggesting that HY and LY rats differ in both of them.

Although pilocarpine diminished novelty- and water immersion-induced grooming of both strains of rats, with a higher sensitivity to this drug shown by HY rats, the inhibition was more marked in the novel than in the water immersion condition. This indicates that the inhibitory influence of this drug depends on the manipulation to which the animals are previously subjected. In addition, pilocarpine seems to inhibit grooming by disrupting mainly body washing, which is a transitional element between rostro and caudal components and also a crucial element in HY grooming structure.

Conversely, pilocarpine appears not to affect indivichial LY grooming components, but all of them to a similar degree. This is probably because LY grooming structure as a whole is more resistant to modification even after immersion in water, in which we observed greater number of grooms, this leaves ont any possibility of statistical bias due to the occurrence of few events. The pharmacological effect of pilocarpine was due to a direct influence on grooming response rather than to a generalized inhibition of locomotor activiiy, as reflected by the finding that activity in open field was not affected by this drug suggesting a specific effect on grooming. The fact that pilocarpine at closes of 3.75 mg/kg induced chewing response, which has been proposed as a reliable index of central muscarinic agonist activity in rats, indicates that it affected mostly central cholinergic activity. In addition, the doses of pilocarpine used in this study are within those (0.5-10 mg/kg) frequently found in other reports on yawning and are below those currently used to produce massive effects.

The genotypic variation in grooming and yawning between HY and LY rats may be the result of differences in the expression of cholinergic neurotransmission and ils interaction with other systems, as several neurotransmitters have been evidenced in other, comparative studies in inbred strains of rodents (7). Resulis,,from our laboratory raise the possibility that HY may have a high~r cholinergic tone than LY rats (34). However, the differences in grooming and yawning bctween HY and LY rats cannot be dependent only on the effect of pilocarpine, because in contrast with the inhibitory effect on grooming, that on yawning is a dose-dependent increase in both sublines of animals. The cholinergic system affects these behaviors in opposite directions and probably along distinct pathways. In fact, the cholinergie neurons involved in yawning are thought to be influenced by dopaminergic rienrons (38). The results presented here are not conclusive on the type of muscarinic receptors, which pilocarpine is mostly affecting, and il is likely that other neurotransmitter systems are involved in the production of grooming.

There is evidence that ACTH, in vitro, inhibits the quinuclidinylbenzilate (muscarinic antagonist) receptor-binding. This might account for the increase of the acetylcholine turnover rate after central administration of ACTH. This is consistent with the finding that inhibition of muscarinic receptor binding in the brain may lead to an increased release of acetylcholine. Therefore, we expected pilocarpine to increase grooming, which contrasts with the results reported here. On the basis of these experimental findings, it appears that the effects of pilocarpine and ACTH on grooming differ, a hypothesis that has been suggested for yawning too. The situation is even more intricate than il may appear since the sole i.c.v. administration of pirenzepine or AFDX-116, selective antagonists of M1 and M2 muscarinic receptors respectively, does not modify grooming behavior in rat, but decreases yawning. Furthermore, the administration of scopolamine in hamsters receiving artificial cerebrospinal fluid did not change grooming. However, some authors have reported that not only muscarinic but also nicotinic receptors are involved in ACTH-induced grooming. We are currently attempting to test whether the differences in grooming between HY and LY rats also involve peptidergic influences. Initial results indicate that HY and LY rats differ in their grooming response to the administration of ACTH.

In conclusion, these results have revealed evidence for a significant genotypic variation in grooming response between IIY and LY rats as well as differences in sensitivity to the behavioral effects of pilocarpine. This difference parallels that of yawning which makes HY rats to be an excellent tool for studying neurochemical mechanisms involved in the generation of both behaviors, and their implications in stressful circumstances.



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