mystery of yawning
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Yawning: its cycle, its role
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Fetal yawning assessed by 3D and 4D sonography
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Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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14 novembre 2010
Dev Psychobiol
2011;53(2):105-117
Comparative analysis of maternal care in the high-yawning (HY) and low-yawning (LY) sublines from sprague-dawley rats
 
Ugarte A, Eguibar JR, Cortés MD, León-Chávez BA, Melo AI.
 
Instituto de Fisiología, Benemérita Universidad Autónoma de Puebla, Mexico.
 
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren

Chat-logomini

Abstract
 
High- and low-yawning rats (HY and LY) were selectively bred as a function of their spontaneous yawning frequency with the LY subline about 2 yawns/hr and the HY 20 yawns/hr. The HY rats have more grooming bouts and travel longer distances in an open field. HY dams spent less time in the nest, retrieved their pups faster, and show a longer latency to licking and mouthing the pups than the LY or outbred Sprague-Dawley (SD) animals. The percentage of HY dams that had atypical retrieving was higher, with a lower nest quality, and produced offspring whose weights were lower than those from the LY subline. We also showed that the pregnant HY dams have fewer pups and the percentage that had lost at least three pups during lactation was higher than the SD and LY dams. In conclusion, HY dams are motivated to take care of their pups, but the "fine tuning" of maternal care is disturbed.
 
INTRODUCTION
 
Social interactions among members of a community are important for their organization and survival. These interactions need the display of affiliative behaviors such as maternal care, sexual behavior, and grooming, compared to the antagonistic ones such as aggression, isolation, and submissive behaviors. In altricial species, maternal behavior is the most important and most studied behavior not only because it allows the immature offspring to become independent over time, but it is also a good model for the offspring's physiological, neuroendocrine, and cognitive display as adults (Beach & Jaynes, 1954; Hofer, 1994). Maternal behavior is the expression of a series of motor and somatosensory events by the mother at the end of pregnancy, parturition, and during the postnatal preweaning period (Rosenblatt, 1967; Rosenblatt & Lehrman, 1963). In rodents, once the pups are born, the mother retrieves them to the nest, licks their bodies and the anogenital region followed by a nursing posture over them in a highly stereotyped and defined organization (González-Mariscal & Poindron, 2002; Rosenblatt & Lehrman, 1963). Thus, the offspring receive warmth, nutrients, protection, and sensory and social stimulation in the form of social contact with the mother and their siblings (Beach & Jaynes, 1954; Hofer, 1994; Levine, Haltmeyer, Karas, & Denenberg, 1967).
 
In rats and mice, differences in the timing and components of maternal behavior have been described over the course of the nurturing period, variations that mediate behavioral transmission of traits and thus transgenerational or nongenomic transmission to the offspring (Champagne, Francis, Mar, & Meaney, 2003; Fleming et al., 2002). There are variations in mother-infant interactions within a same strain, that is, natural variations (Champagne, Curley, Keverne, & Bateson, 2007; Champagne et al., 2003; Meaney, 2001). For example, by choosing the extremes of the populations of the Long-Evans rats and comparing the frequency that the mothers lick their pup's body and genitals, and their nursing posture, Meaney and his group had found that there are mothers that show high levels of licking and arched-back nursing (HG-ABN) and other mothers that show low levels of these behaviors (LG-ABN; Champagne et al., 2003).
 
Interestingly, lactating rats from HG-ABN mothers show a low reactivity of the hypothalamus-pituitary-adrenal (HPA) axis after exposure to stressful environment, with a small fear response, a good level of spatial learning, and mainly spent much time licking and nursing their pups compared to the LG-ABN dams. These differences are not caused by the genetic background because cross-fostering studies have shown that the offspring phenotypes depend on the mother that reared it (Champagne et al., 2003). Experimentally, it is possible to regulate how the mothers take care of their offspring. If lactating rats are exposed to a handling paradigm (pups are removed from the nest for 15 mm), the dams spend more time licking the body and genital area of the pup's when they are returned to the nest (Meaney et al., 1985; Pryce, Bettschen, & Feldon, 2001). Contrary to the handling paradigm, mothers who had been isolated from their mothers during infancy spent less time taking care of her pups (Gonzalez, Lovic, Ward, Wainwright, & Fleming, 2001; Melo, HernándezCuriel, & Hoffman, 2009; Melo et al., 2006). Different groups of mice showed remarkable variations in the expression of maternal behavior (Anisman, Zaharia, Meaney, & Merali, 1998; Broida & Svare, 1982; Brown, Mathieson, Stapleton, & Neumann, 1999; Champagne et al., 2007; Ohta, Shirota, Tohei, & Taya, 2002; Shoji & Kato, 2006).
 
Thus, lactating female mice of CS7BL/6, CBAIH, C3FIJIco, and CBAIJ strains retrieved pups faster than BALB/c, NBZ, DBAI2, XLII, NJ, and AKR strains (Carlier, Roubertoux, & Cohen-Salmon, 1982). Furthermore, DBAI2J females built better nests and spent more time crouching over and nursing pups (Brown et al., 1999) than CS7BL/6J dams.
 
A comparison between inbred and outbred mice has shown that the 129Sv strain had shorter latencies in nest building, built the nest less frequently, and spent less time engaged in licking the pups than outbred dams (Broida & Svare, 1983; Champagne et al., 2007; Meaney, 2001). In rats, psychogenetic selection has resulted in at least four different strains that, besides their own phenotype, have variations in postpartum maternal behaviors; (1) The Flinders Sensitive Line (FSL), considered a genetic animal model of depression, spent less time licking the
 
pups and nursing them (Lavi-Avnon, Yadid, Overstreet, & Weller, 2005), a shorter latency to first pup retrieval, and more self-directed behavior than controls (Braw et al., 2009); (2) spontaneously hypertensive rats (SHR) more often had an arched and blanket-nursing posture and a lesser passive-nursing posture, spent less time licking their pups, and retrieved them more quickly than the Wistar strain (Myers, Brunelli, Squire, Shindeldecker, & Hofer, 1989); (3) Roman high (RHA-Verh)- and low (RLA-Verh)-avoidance sublines of rats were selected and bred for their rapid response compared to poor acquisition in a two-way active-avoidance response (Steimer, Escorihuela, Fernández-Teruel, & Driscoll, 1998). Female rats of RHA-Verh mothers had a high active avoidance, spent less time with their young, are more active, and also assumed the side-nursing position less often than the RLA-Verh mothers (Driscoll, Fumm, & Bàttig, 1979); and (4) Hatano high- (HAA) and low- (LAA)-avoidance selective-breeding lines from the Sprague-Dawley strain (Ohta, Matsumoto, Nagao, & Mizutani, 1998) show a high variation in the expression of maternal behavior, with the low avoidance (LAA) females having longer latencies for retrieving the pups, spent less time with them, showed a decreased amount of milk ejection, a lesser increase in blood prolactin, and a greater increase of adrenocorticotrophic hormone (ACTH) than the HAA mothers (Ohta et al., 2002).
 
Although the behavioral differences among inbred groups of mice or rats are attributed to genetic variations, it has been reported that the genetic-environment interactions early in life, mainly mediated by maternal care and their siblings, are the main cause of those variations (Francis, Szegda, Campbell, Martin, & Insel, 2003; Myers et al., 1989; Ohta et al., 1998; Shoji & Kato, 2009; Steimer & Driscoll, 2005). These data show that, besides the phenotype used, during inbreeding the process can generate other changes of the behavioral display that could be caused by maternal care.
 
Yawning is a phylogenetically old behavior and stereotypically shown by reptiles, fish, birds, and mammals (Walusinski & Deputte, 2004). It consists of a wide opening of the mouth with a long inspiration, followed by a short expiration. Yawning can be modulated by several peptides such as adrenocorticotropin hormone, alpha-melanocyte stimulating hormone, and oxytocin, and also by several neurotransmitters as GABAergic, dopaminergic, and muscarinic cholinergic systems in several strains of rats, as well as HY and LY sublines (for review, see Collins & Eguibar, 2010; Doger, UrbáHolmgren, Eguibar, & Holmgren, 1989; Eguibar, Barajas, & Moyaho, 2004; Eguibar, Romero-Carbente, & Moyaho, 2003; Urbá-Holmgren, Santos, Holmgren, & Eguibar, 1993). The HY males yawned more and also had more grooming bouts after exposure to a novel environment than LY rats (Eguibar & Moyaho, 1997). The HY subline is also more active in an open-field arena (Moyaho, Eguibar, & Diaz, 1995). In addition, after wetting the HY showed a disorganized grooming-chain sequence compared to the LY animals with a clear cephalocaudal organization, similar to that obtained in other strains of rats (Moyaho et al., 1995). These observations suggest that the early life experience, such as maternal care and lactation, could be the cause of the differences among the sublines. In our experiments, we analyzed maternal care toward their own offspring of HY and LY dams and compared them with outbred Sprague-Dawley dams during the early-to-middle lactation period. In a second experiment, we compared the number of pups at parturition and weaning and the fertility index of the females of all groups.
 
DISCUSSION
 
In this study we compared the maternal and nonmaternal behaviors of primiparous female rats of the HY and LY inbred sublines compared to outbred Sprague-Dawley rats during early-to-middle lactation. Our results showed that HY mothers express different patterns of maternal and nonmaternal behaviors compared to the SpragueDawley and LY dams. In addition, the number of pups per litter at birth and weaning from the HY mothers was lower compared to the other groups of rats.
 
The results showed that the time engaged in nursing and licking the pups did not significantly differ among the groups, but the HY and LY mothers spent less time inside the nest than the Sprague-Dawley dams. In contrast, the HY dams retrieve all pups to the nest more quickly than the Sprague- Dawley mothers. These results are similar to that obtained in mice from the C57BL/6, CBAIH, C3W Ico, and CBAIJ strains, which retrieved pups more quickly than the BALB/c, NBZ, DBAI2, XLII, NJ, and AKR strains (Carlier et al., 1982). The HY dams not only retrieve the pups more quickly, but most of them made atypical retrievings and also displayed reretrieving and built the nest more rapidly, but with lower quality. These results match with those found in the 129Sv inbred strain that had shorter latencies in nest building, built the nest less frequently, and spent less time in licking the pups (Champagne et al., 2007). The above data suggest that mothers are maternally motivated but the "fine tuning" of the expression of all maternal characteristics are disturbed, similar to that already reported in the organization of grooming bouts in HY rats (Eguibar & Moyaho, 1997; Moyaho et al., 1995). Interestingly, when we compared the latency of each maternal component in the early compared to the middle lactation, we showed that mothers from all groups showed similar latencies during the early lactation. During the middle lactation the latency to retrieve the pups, mouthing them, and building the nest by the HY dams was shorter, but the latencies to begin licking the body and genital areas of the pups were longer than that of the LY and Sprague-Dawley dams.
 
The HY, the LY, and the Sprague-Dawley dams showed normal maternal motivation because once they get cues from the pups, they established contact with them (appetitive component), then they walk around the maternal cage with the pups in their mouth and put them in a different place and later on reretrieve them to the nest. This shows that they have enough motivation to engage in a behavioral interaction with a specific goal object, and they retrieve them to the nest (consummatory component), but their ability to show a specific behavior, that is, properly retrieve the pups is not adequate after putting them outside the nest, reretrieve them and also with atypical retrieving suggesting a disorganized pattern in the global organization of maternal care in HY rats (Everitt, 1990; Numan, Fleming, & Levy, 2006; Numan & Insel, 2003; Timberlake & Silva, 1995). The HY males also have a disorganized sequence of their grooming bouts because they showed caudocephalic or lateralcaudal sequences, instead of the cephalocaudal sequences shown by the LY rats and other rodent species (Berridge, 1990; Moyaho et al., 1995). These alterations could be caused, at least in part, to a greater number of D1 dopaminergic receptors in the ventral striatum in the HY compared to the LY animals (Diaz-Romero, Arias-Montaflo, Eguibar, & Flores, 2005). Matell, Berridge, and Wayne-Aldridge (2006) showed that the grooming syntactic chains can be altered after a lesion of the striatum or changing the dopaminergic transmission in the nigrostriatal pathway. It is well known that the basal ganglia play a crucial role in the organization, timing, and coordination of motor sequences including grooming (Cromwell & Berridge, 1996). Furthermore, systemic administration of SCH23390, a specific dopaminergic D1 antagonist, produced a disruption of maternal care causing the mother to leave the pups outside the nest, so reretrieving them (Byrnes, Rigero, & Bridges, 2002). This also happens with intraaccumbens injection of cis-flupenthixol, which inhibits maternal retrieving and licking the pups but enhances nursing behavior in lactating Long-Evans rats (Keer & Stern, 1999). The maternal-care deficits caused by haloperidol can be restored by demanding pups (12-hr deprived), showing that pups can reverse the effects produced by the dopaminergic antagonist and by bromocriptine, a dopaminergic agonist that produced an opposite effect (Pereira & Ferreira, 2006). Because the HY rats showed an increase of D1 receptors in the ventral striatum (Diaz-Romero et al., 2005) and a decrease in the dopamine levels in the nucleus accumbens (unpublished data), we suggest that dopamine changes could be responsible for the alterations in maternal care in the HY dams.
 
Recently, it has been reported that the mother not only gives somatosensorial stimulation but also gives growth factors such as prolactin and growth hormone through the milk that could act in concert to aid growth, weight gain, and glucose homeostasis in the perinatal period (Fleenor et al., 2005). Prolactin plays a fundamental role not only to support milk production but also in the developmental and maturation of the pups (Melo et al., 2009). The above data suggest that because that HY offspring never gain normal weight during lactation it could be that these dams produce milk of lower quantity or quality. It is also possible that humoral factors such as growth, oxytocin, and thyroid hormones could be responsible for the lower rate of body-weight gain in the HY offspring (Bautista, Boeck, Larrea, Nathanielsz, & Zambrano, 2008; Glinoer, 1997; Hapon, Simoncini, Via, & Jahn, 2003; Valdez, Penissi, Deis, & Jahn, 2007).
 
A relationship between high emotionality and a deficit in the expression of maternal licking and grooming as well as arched-back nursing posture has been demonstrated (Francis, Diorio, Liu, & Meaney, 1999; Gonzalez, Lovic, Ward, Wainwright, & Fleming, 2001; for review, see Numan & Insel, 2003). Female rats that are isolated early
 
in life had a high stress response and show a deficit in the expression of maternal behavior, and these characteristics are transmitted to the next generation (Gonzalez et al., 2001).
 
Because the HY offspring have lower weights during lactation that persists until adulthood, it is possible that behavioral disturbances found in these rats could be caused by differences in the maternal care, including grooming and the arched-back posture. There are some reports that partially support this hypothesis, that is, mothers that were undernourished during early life had an abnormal maternal care, as we found in the HY mothers. Thus, these dams show a decrease in nest quality and nursing time, an increase in the latency to retrieve pups, and atypical retrievings that can even produce sonic distress in the pups (Regalado, Torrero, & Salas, 1999; Salas, Torrero, Regalado, & Perez, 2002; Salas, Torrero, & Pulido, 1984; Smart, 1976). The HY mothers also had a lower nest-building rating and showed atypical retrievings. Rosenblatt and Lehrman (1963) reported that when a female cannot maintain a stable nest, she retrieves the pups too many times and deposits them anywhere in the cage, similar to that made by HYand LY dams, suggesting that the sublines had a disorganized pattern of maternal care.
 
It is important to emphasize that body weights of undernourished pups from 4 to 20 days old were about 20-50% lower than well-nourished rats (Bautista et al., 2008; Salas et al., 1984,2002; Wiener, Fitzpatrick, Levin, Smotherman, & Levine, 1977; Zambrano et al., 2005). We found that body weights in the HYoffspring were 16-25% lower during lactation compared to the Sprague-Dawley and LY animals. Because of the ad libitum disposition of rodent food pellets the disturbed expression of maternal behavior in HY dams are not because they are being underfed during neonatal period, but it is probably generated by maternal care. These deficits in birth weight can be corrected by improving postnatal nutrition, as reported in Wistar Kyoto rats, a good model of anxiety responses (Romano, Wark, Owens, & Wlodek, 2009). In our experiments the animals have free access to food (Zeigler) with 22% protein, but they did not reach weights similar to Sprague-Dawley pups surely because of their genetic background (Moyaho et al., 2009). The "fetal origin hypothesis" proposes that prenatal environmental exposures, including maternal stress, could have sustained effects across the lifespan (Kinsella & Monk, 2009). A positive correlation of food ingestion during pregnancy and low body weight in their offspring has been demonstrated (Massaro, Levitsky, & Barnes, 1974; Passos, Ramos, & Moura, 2000), including women with a poor diet before and during pregnancy who had babies with a low birth weight (Lechtig et al., 1975), and where the frequency of infant mortality is four times higher than normal birth weight babies (Habicht, Yarbrough, Lechtig, & Klein, 1973).
 
Comparisons among inbred strains of rodents are important to determine the effect of environmental factors over behavioral traits made under laboratory conditions. Thus, environmental manipulations such as maternal separation early in life, handling, and enriched environments clearly affect subsequent juvenile or adult performances (Fleming et al., 2002). As in many other inbred strains of rodents, work has focused on the participation of genetic and epigenetic factors involved in the development of specific behaviors (Francis et al., 2003). The HY offspring had fewer contacts with their mothers, receive less grooming, and were retrieved carelessly (atypical retrievings and reretrievings), similar to that reported in stressed mothers (Salas et al., 2002). The HY mothers have fewer pups per litter at parturition, most of them lost pups during lactation, and the mean weight of their pups is lower from birth to weaning compared to the LY and Sprague-Dawley offspring. These behavioral differences could be caused by some metabolic, hormonal, or emotional issues during pregnancy or lactation (Fleenor et al., 2005; Glinoer, 1997; Hapon et al., 2003; Ozzane & Hales, 1999; Shono, Imagima, Zakaria, & Suita, 1999). Pups, exposed to dexamethasone by its injection into their mothers during pregnancy, produced an offspring with lower weight and chronic hyperactivity of the FIPA gland axis. These pups had higher plasma-corticosterone levels with an upregulation of hepatic gluconeogenesis and insulin resistance suggesting that glucocorticoids levels are a key factor for metabolic activity as adults (Buhl et al., 2007; Burlet et al., 2005).
 
The release of oxytocin in the paraventricular nucleus (PVN) of the hypothalamus at parturition probably facilitates a positive feedback in both parvocellular and magnocellular neurons to coordinate the high levels of oxytocin release that are important for the generation of maternal behavior, infant recognition, and bonding (Carter & Keverne, 2002). This is also true for yawning expression because the release of oxytocin in the PVN is a key factor for the generation of yawning, not only by this peptide, but also in this part of the brain the dopaminergic, excitatory amino acids, nitric oxide, GABA, and opioid receptors converge to increase yawning frequency, suggesting that neural mechanisms in the hypothalamus are important regulators for yawning and pair bonding (for review, see Collins & Eguibar, 2010). Preliminary results showed that HY rats yawned more after the i.c.v. injection of oxytocin than the LY animals, but with similar grooming scores (unpublished data), suggesting different sensitivities in the neural pathways that mediate these behaviors. In future experiments, we will address oxytocin levels during parturition and lactation in both sublines.
 
In conclusion, our results were that the HY dams showed a different organization of maternal care with a reduced litter size and lower weights of pups at parturition and weaning. These changes can be caused by hormonal or neural mechanisms, which are able to alter somatosensory stimulation of the pups and also can produce hormonal and metabolic changes that ultimately are responsible for different behavioral characteristics of HY rats, such as yawning and grooming sequences in the adults.