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19 mai 2015
Exp Brain Res
2015;233(7):2073-80
Electrophysiological association of spontaneous yawning and swallowing
 
Ertekin C, Bulbul NG, Uludag IF, Tiftikcioglu BI, Arici S, Gurgor N.
 
Departments of Neurology and Clinical Neurophysiology, Medical School Hospital, Aegean University, Bornova, Izmir, Turkey

Chat-logomini

 
Occurrences of Yawn and Swallow are Temporally Related Abe Kimikos, Weisz SE, Dunn RL, et al.  2014
 
Abstract
 
Yawning and swallowing are fundamental physiological processes that are present from fetal stages throughout life and that involve sequential motor activities in the oropharyngo-larynx making it likely that they may share neuroanatomical pathways. We postulate that yawning and swallowing are controlled by a distributed network of brainstem regions including the central pattern generator of swallowing, and therefore spontaneous swallowing is frequently associated with spontaneous yawning. In this study, we sought to test this hypothesis by evaluating the elementary features of yawning in the facial, masseter and submental muscles, together with laryngeal movement sensor and respiratory recordings for spontaneous swallowing. We investigated 15 healthy, normal control subjects, 10 patients with Parkinson's disease (PD) and 10 patients with brainstem stroke (BSS). Apart from four subjects with PD and two with BSS, who had dysphagia, none of the other study subjects were dysphagic by published criteria. Twenty-five subjects (10 control, 10 BSS, 5 PD) were evaluated by 1-h polygraphic recording, and 10 (5 control, 5 PD) underwent whole-night sleep recordings. One hundred thirty-two yawns were collected, 113 of which were associated with spontaneous swallows, a clear excess of what would be considered as coincidence. The yawns related with swallows could be classified into the following three categories. The characteristics or the duration of swallows and yawns were similar between controls and disease subjects, with the exception of increased duration of yawning in subjects with BSS. Our findings support the presence of common neuroanatomico-physiological pathways for spontaneous swallows and yawning.
 
Introduction
 
Yawning is an involuntary and stereotyped behavior common to several vertebrate species besides humans. It occurs from fetal stages to adulthood (Baenninger 1997; Walusinski and Deputte 2004; Provine 2005). One of the best descriptions of yawning in humans was reported by Barbizet (1958) as a complex, involuntary and paroxysmal movement.
 
It is a motion unfolding itself in a certain order wherein three phases may invariably be distinguished. The first one is active and inspiratory; the second phase corresponds to the acme; and the third phase is passive and expiratory (Barbizet 1958). Yawning occurs about 7&endash;8 times per day in adult human subjects with a range of 0&endash;28. It is more likely to take place during wake&endash;sleep and sleep&endash; wake transitions. It may also occur during boredom and the onset of hunger and satiety (Barbizet 1958; Provine and Hamarnick 1986; Walusinski 2009).
 
When we look at yawning from the view of the oropharynx and respirations, the three phases of yawning described by Barbizet (1958) should be very important for breathing and spontaneous saliva swallowing. In the first phase, there is a progressive slow opening of the mouth while the dilatation of the pharynx, larynx and thorax and lowering of the diaphragm muscle can be shown by radiological methods. The second phase of yawning corresponds to the acme of the mouth's opening and to that of pharyngeal and thoracic dilatation. Facial modification begins at the end of the first phase. Contraction of the lip dilatators exaggerates the mouth's opening, and contraction of the eyelids causes a partial or even total occlusion of the eyes. At this phase, partial or general stretching could also be observed particularly on the neck and trunk extension including hyperextension of the limb muscles. The third phase is passive, where inspirium ceases abruptly and expiration is slow. Pharynx goes back to its normal size, mouth closes spontaneously, and the face resumes its usual aspects.
 
During these 5&endash;7 s, we may expect a highly significant amount of sensory input to the brainstem from ponto-bulbar and upper spinal cord (Ertekin et al. 2000; Ertekin and Aydogdu 2003; Ertekin 2014). Additionally, increased salivary flow associated with yawning was reported (Inomata et al. 2005). Duration of yawning was reported as 4&endash;7 s (Barbizet 1958) and even as long as 5&endash;10 s (Askenazy 1989; Walusinski 2009). Thus, it is possible that spontaneous saliva swallowing could overlap with yawning within this duration or that the physiological nature of yawning could elicit spontaneous swallowing. There are likely to be similarities between the neuroanatomical pathways utilized in yawning and spontaneous saliva swallowing both of which involve the oropharynx and larynx. It is probable that the same ponto-bulbar and upper cord afferents and their receiving nuclei are involved in both activities. Swallowing occurs mostly in non-REM-1 and non-REM-2 stages of sleep (Sato and Nakashima 2006; Ertekin et al. 2013). Similarly, yawning was often observed in the same stages of sleep. Thus, yawning and swallowing may be controlled by a distributed network of brain stem regions including the central pattern generator (CPG) of swallowing (Cattaneo et al. 2006; Zilli et al. 2008; Walusinski 2009). Therefore, our hypothesis is that spontaneous saliva swallowing is frequently associated with spontaneous yawning.
 
Another piece of evidence in support of this hypothesis comes from Parkinson's disease (PD) and other parkinsonian disorders. There are reports that certain extrapyramidal syndromes are accompanied by the disappearance of yawning such as patients under neuroleptic treatment (Mogulnicka and Klimek 1977) and PD (Clossimo and Pontieri 1999). The treatment by apomorphine, a rapidly acting dopaminergic stimulant, is observed to trigger yawning during the "off" period in PD (Blin et al. 1990; Kolls and Stacy 2006). Yawning difficulties were described in progressive supranuclear palsy (PSP) which were treated by dopamine agonists (Sandyk 1987). Importantly, there are a considerable number of PD and brainstem stroke (BSS) patients with dysphagia (Ertekin et al. 2002; Ertekin 2014; Kalf et al. 2012; Michou et al. 2013 and many others for PD and Horner et al. 1991; Daniels et al. 1999; Aydogdu et al. 2001; Smithard 2002 for BSS).
 
Thus, studying the relationship between yawning and swallowing in subjects with parkinsonian disorders as well as healthy controls can provide clues about the relationship of these fundamental processes in health and disease.
 
Thus, we postulate that yawning and swallowing are controlled by a distributed network of brainstem regions including the central pattern generator of swallowing, and therefore spontaneous swallowing is frequently associated with spontaneous yawning. Therefore, we studied by evaluating the elementary features of yawning in the facial, masseter and submental muscles, together with laryngeal movement sensor and respiratory recordings for spontaneous swallowing. To our knowledge, relationship between spontaneous yawning and swallowing has not hitherto been studied in health and disease using such thorough neurophysiological assessment.
 
Discussion
 
In this study, 132 spontaneous yawns from 35 normal controls and patients were individually investigated. Only 19 yawns were not found to be associated with spontaneous swallows. This may be due to methodological artifact; because the EMG of yawning in the OC, OR, MS and SM muscles often had crescendo and later decrescendo interference patterns with high amplitude, the swallowing pattern of the related muscles could not be distinguished. Furthermore, sometimes the laryngeal sensor was disturbed by maximal opening of the mouth, and swallowing pattern could, therefore, not be distinguished easily from the traces. Additionally, due to the low incidence of yawning, some saliva swallows could be missed by the examiners. All of these technical issues could have resulted in the low yawning&endash; swallowing association during the yawning period This means that about 86 % of spontaneous yawning is associated with spontaneous swallows. Hence, these two oropharyngo- respiratory spontaneous behaviors are often but not always associated with each other. The high incidence of spontaneous yawning associated with swallowing is compatible with these two oropharyngo-laryngeal behaviors.
 
The anatomophysiological conditions produced by spontaneous yawning underscore the physiological nature of this association. Spontaneous yawning is a complex act consisting of a long inspiration phase that comprises of mouth opening, dilatation of pharynx, larynx and thorax and diaphragm together with a brief interruption of ventilation and final expiration phase which involves the relaxation of all participating muscles (Barbizet 1958; Baenninger 1997; Provine 2005). During the inspiratory period of yawning, there is a strong possibility that the saliva accumulated in the oral cavity or escaping to the pharynx triggers a swallow. It has been shown that inspiration is prolonged in duration when swallowing takes place during the inspiratory phase of respiration. Despite this, the EMG activity of the diaphragm does not cease with swallowing during inspiration (Uysal et al. 2013). During prolonged inspiration, it is easier to record spontaneous swallows overlapping with the yawning period. Nearly 18 % of spontaneous yawning was associated with a swallow within its action period. In reality, this number must be higher, but technically during the maximal opening of the mouth, we could neither observe nor record associated swallows. This is because there is a crescendo type of increase in the EMG amplitudes of related muscles of yawning leading to a tremendous peak, in parallel with the clinical mouth opening. Therefore, in this part of yawning, it is not possible to clearly visualize swallowing-related muscle activity. The second mode of association with swallowing that occurs right at the end of yawning was the most frequently encountered relationship between these two spontaneous oropharyngeal behaviors. The end of the yawn and the onset of the swallow are rather close to each other. Clinically, at the end of closing of the mouth, swallowing can appear in this mode of association.
 
Why is spontaneous yawning frequently associated with spontaneous saliva swallows? Despite lack of clear evidence, we may postulate that the tremendous inputs coming from many muscles innervated by the lower motor cranial nerves (V, VII, IX, X, XI and XII) and the cervical (C1&endash;C4) and thoracic cord (intercostal nerves) have already been excited by about 6 s of yawning. It is well known that the nuclei of the motor cranial nerves are situated in the pontomedullary region. Given that there is a sequential muscle activation from cranial to caudal direction in the yawning behavior, it is likely that this is organized at the premotor level, like the central pattern generator (CPG) of swallowing situated at the nucleus tractus solitarii (NTS) and nucleus ambiguous (NA) with a link to respiratory rhythm center as pre-Bötzinger complex. (Jean 2001; Ertekin and Aydogdu 2003; German et al. 2009; Lang 2009; Ott et al. 2012; Ertekin et al. 2013). It is probable that spontaneous yawning activity is organized at similar neural structures as for swallowing, and the higher excitability of premotor neurons during yawning leads to the secondary behavior of swallowing. Since brainstem circuits are involved in the sensorimotor control of multiple functions including respiration, mastication and swallowing (Jean and Dallaporta 2006; German et al. 2009), both yawning and swallowing may be under the control of similar brainstem circuitry. Furthermore, increased salivary flow in association with yawning has been reported (Inomata et al. 2005), which may also increase the excitability of the swallowing CPG neural network. This may produce firstly the spill of saliva through pharynx during the yawn. It is conceivable that just after yawning and within 2 s of its termination, a prolonged and rhythmic excitability of the CPG might produce later Materials and swallows (Nakamura et al. 2004; Aydogdu et al. 2011). We also detected increased saliva accumulation associated with yawning in our patients with PD, as previously shown (Kalf 2011).
 
Yawning is classified into two types as spontaneous and contagious yawning. Both types are similar in their motor action and their triggering mechanism, although their evolutionary nature and social meaning are different (Provine and Hamarnick 1986; Baenninger 1997). Abe et al. (2014) reported that contagious yawn and swallow are temporally related, and frequency of yawn was increased within 10 s of post-yawn period in normal adult subjects. Our study is principally different than that of Abe et al. as we describe and demonstrate qualitative and quantitative features of spontaneous yawning associated with swallowing, from the onset to the end of yawning and within a 2 s window after the end of a yawn. The main conclusion from the Abe et al. study was the identification of the increased rate of swallowing after contagious yawning. Although it was previously described that two patients had inhalation of foreign bodies into their bronchi which manifested as suffocation (Evans 1978), spontaneous yawning associated with swallows seemed to be safe for our patients. We did not observe any clinical signs of aspiration such as coughing just after yawning, even in our six patients with neurogenic dysphagia.
 
In conclusion, spontaneous yawning and swallowing are often but not always associated with one another. Normal controls and patient groups did not differ in their yawning and swallowing features by clinical and electrophysiological methods. Quantitatively, the EMG duration of yawning was significantly prolonged in the BSS group. This is probably due to the fact that both spontaneous yawning and spontaneous swallowing are operated within the brainstem. Finally our electrophysiological findings support the presence common neuroanatomico-physiological pathways for spontaneous swallows and yawning.