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 mise à jour du
30 septembre 2002
Behavioural Brain Research
1990; 40; 29-35
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 Genotypic dependency of spontaneous
yawning frequency in the rat
R Urba-Holmgren, N Trucios, B Holmgren, JR. Eguibar, A Gavito, G Cruz, G Santos
 Departamento de Ciencias Fisiolbgicas, Instituto de Ciencias, Universidad Autônoma de Puebla, Puebla (Mexico)
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren


The mid-twentieth century reviews on yawning by Heusner (1946) and Barbizet (1958 ) offered adequate coverage of earlier literature on this ubiquitous and apparently trivial behavioral pattern. Apart from a burgeoning of research in the twenties on the physiological mechanisms involved in yawning and on some pathological conditions with which it might be associated, specially by German authors this field has continued to be rather neglected until our day. Even if the mechanisms underlying yawning are far from properly elucidated, and its biological significance is largely ignored, important advances in its understanding may be anticipated, due to the increasing number of research groups, especially among neuropharmacologists, paying attention to this motor act.

In 1955 Ferrari et al.were fortunate enough to come upon a peculiar behavioral syndrome: when dogs were intracerebroventricularly injected with a commercial preparation of adrenocorticotrophic hormone (ACTH), after a latent period of about 30 min, the animals started to yawn andstretch very frequently. This was the first report on pharmacological induction of yawning. Some years later, this Italian group extended their observations to other animal species and demonstrated that the stretching-yawning syndrome (SYS) was elicitable both by ACTH and melanocyte-stimulating hormone (MSH). Since in these early experiments they showed the antagonistic effects of atropine and scopolamine on SYS, they suggested that a cholinergic mechanism might be involved. More than a decade later several authors demonstrated that other neurotransmitter-related drugs also had yawning-inducing effects and that most (if not all) of them seemed to involve a cholinergic mechanism, as judged by their susceptibility to muscarinic blocking drugs.

In recent years it has been suggested that elicitation of yawning is mainly the result of an interaction, somewhere in the brain, between inhibitory dopaminergic and excitatory cholinergic influences on the built-in motor program. for yawning. Yawning elicited by low doses of apomorphine and other dopamine (DA) agonists has most generally been interpreted as the result of their selective action on low-threshold DA autoreceptors regulating impulse discharge, synthesis and liberation of the neurotransmitter. Nevertheless several authors have postulated that the yawn-inducing effect of low doses of DA agonists is a postsynaptic excitatory effect upon exquisitively sensitive DA2 receptors. Higher doses of DA agonists would decrease yawning by acting directly on high-threshold postsynaptic DA yawninhibitory receptors.

Moreover, there are several other neurotransmitter and hormonal mechanisms known to influence yawning, directly or indirectly . Thus, a rather high number of proteins (enzymes, receptors, etc.) may be involved in the regulation of this behavioral pattern. Therefore, it could be expected that some differences in the level of spontaneous yawning frequency might have a genetic background.

By inbreeding we have developed 2 Sprague-Dawley sublines: one of them yawns spontaneously at a low frequency (LY), the other at a higher level (HY). We describe the evolution of this behavioral pattern along the first year of life in both sublines and the results of reciprocal crosses between them. [...]

Discussion : Research in yawning behavior has moved during the past decade from a rather neglected position to become a field of rapidly growing interest, particularly for neuropharmacologists. With the aim of developing better experimental subjects for the physiological analysis of this behavior, we have endeavoured to obtain inbred genetic sublines of Sprague-Dawley rats with high and low spontaneous yawning rates.

The increase in yawning activity in HY males was observed from the very beginning of inbreeding, the differences between homologous generations of HY and LY rats being highly significant from F3 onwards. Yawning activity in HY females is slightly but significantly higher than in LY females. In both sublines females yawn much less than males, confirming the sexual dimorphic character of this behavior.

We feel it must be stressed that the quantitative data on yawning here reported have been obtained under very strictly standardized observational conditions (see Methods), which have been maintained during almost 8 years. Yawning frequency in HY animals is more susceptible than in LY rats to changes in the conditions under which the animals are observed: it decreases during social interaction with other littermates when animals are placed in collective cages; it increases, due to habituation to being placed singly in novel environments, when observation sessions are repeated at daily intervals; it also has an important circadian variation.

Yawning activity increases with age. Young and adult rats yawn at a higher rate than infant animals. It is well known that at puberty there is an important increase in testosterone levels in male rats and it has been demonstrated that the administration of this sex hormone promotes an important increase in yawning frequency both in female rats and castrated males. However, we have not found any différence in the serum levels of testosterone between HY and LY rats, so we are inclined to discard androgenic hormonal factors as contributors to the difference in yawning rates observed between these two sublines (Eguibar et al., unpublished results).

Biometrical analysis of non-segregating populations (Pl, P2 and FI) after reciprocal genetical crosses between animals of the HY and LY sublines, suggested that one pair of genes is involved in the difference between these sublines and that the LY (P 1) subline is partially dominant over the HY (P2) one. Since no differences were found between reciprocal FI or F2 generations, maternal factors may be excluded.

Yawning behavior is subject to important dopaminergic (inhibitory) and cholinergic (excitatory) influences 15,33. If tonic doparninergic inhibitory control diminishes, yawning frequency increases. The same happens with an increase in cholinergic activity. Thus, on a still rather loose conjectural basis, we think that HY rats may have a higher tonic cholinergic activity than LY animals. An increase in cholinergic tone in HY rats could be understood as a direct and general effect, intrinsic to the cholinergic system as a whole, or an indirect and more particular phenomenon, resulting from a decrease in tonic DA inhibitory activity, and therefore restricted only to cholinergic pathways subject to dopaminergic restraining control. We do not yet have a definite choice between these alternative hypothetical possibilities, which are under current experimental scrutiny with pharmacological tools.