Normal movement of the anterior two thirds of the tongue is essential for carrying out the tasks of the oral stage of swallowing. Tongue musculature can be broadly divided into extrinsic and intrinsic muscles. The extrinsic muscles are the genioglossus, hyoglossus, styloglossus and palatoglossus muscles. These muscles have their origin along the mental spine, hyoid bone, styloid process and soft palate, respectively, and insert either into the hyoid bone or into the other extrinsic or intrinsic tongue muscles. The primary actions of the extrinsic tongue muscles are to pull the tongue forward, backward, upward and downward (3).
The intrinsic tongue muscles are bundles of interlacing fibers containing connective tissue septa. These muscles originate in the tongue submucosa and insert into each other and into the extrinsic tongue muscles in various locations throughout the tongue. The primary action of the intrinsic muscles are to produce changes in the shape of the tongue during articulation and deglutition.
One can see from the variety of origins and insertions of the tongue muscles that to physiologically reproduce these intertwining muscular actions is daunting and inefficient, hence the disparate range of swallowing difficulties necessarily encountered after ablative cancer surgery of the tongue, no matter how sophisticated the reconstruction (4).
While a functioning anterior two thirds of the tongue is critical to normal functioning of the oral phase of deglutition, the posterior one third of the tongue, or tongue base, also plays an important role in the generation of forces that propel a food bolus posteriorly towards the pharynx. Without a functioning tongue base, tongue-soft palate contact can not be made. With impaired tongue-soft palate contact during the oral phase of swallowing, the nasopharynx can not be sealed from the oral cavity so insufficient negative pressure is generated when the hyomandibular complex elevates away from the posterior pharyngeal wall during the pharyngeal phase of swallowing (5). As a result, bolus propulsion becomes significantly impaired.
For normal tongue function to take place both the motor and sensory systems of the tongue must be intact. To assess tongue motor function the tongue should first be examined while at rest along the floor of the mouth with the mouth open. A physical examination demonstrating tongue fasciculation can be the first clue to impaired neurological function in general and impaired neurological function in the tongue specifically (6). To further assess tongue motor function one can assess tongue mobility by having the patient move their tongue superiorly, inferiorly and laterally on command. Tongue strength can be assessed by having the patient press their tongue against a tongue blade or against their buccal mucosa.
Assessment of tongue sensation is also critical to the assessment of the swallow. Using two point discrimination testing, it has been shown that the tongue tip is the most sensitive area of the tongue surface, followed by the lateral dorsal tongue, lateral ventral tongue and floor of mouth (7). Impairment of tongue sensation has been shown to result in major disturbances in oral function, both in healthy controls and in patients with oral cavity cancer (8, 9).
There exist age-related changes in sensory discrimination of the tongue, with people over 60 years of age having a statistically significant less sensitive two point discrimination level in the anterior two thirds of the tongue than people less than 40 years old (10). There also exist age-related changes in tongue motor function with oral transit time in individuals over 60 years of age prolonged when compared to people less than 60 (11). The coupling of the findings of diminished tongue sensory and motor function with increasing age might contribute to the increased prevalence of dysphagia, aspiration and pneumonia seen in the elderly (12, 13). In healthy individuals, the oral phase of swallowing is generally completed in approximately 1 second (14).
Pharyngeal Phase
Once the food bolus encroaches on the palatoglossal folds, or anterior tonsilar pillars, the pharyngeal phase of swallowing reflexively begins. Factors other than the food bolus coming in contact with the anterior faucial arches are thought responsible for the initiation of swallowing, such as posterior tongue movement and stimulation of the pharynx (15, 16). Furthermore, it has been shown in several studies that the swallowing reflex can be initiated entirely by peripheral stimulation of the internal branch of the superior laryngeal nerve (17, 18, 19, 20). The afferent and efferent contributions of the cranial nerves essential for carrying out the pharyngeal phase of deglutition are listed in Table II.
What actually takes place as the swallowing reflex is initiated is as follows:
- Velopharyngeal closure to prevent reflux of material into the posterior choana.
- Closure of the larynx in a specific sequence to prevent aspiration.
- Contraction of the pharyngeal constrictor muscles in a superior to inferior direction.
- Elevation of the larynx and hyoid bone towards the base of tongue.
- Relaxation of the tonically contracted cricopharyngeus to allow passage of the food bolus into the esophagus.
Velopharyngeal closure is effected by contraction of the levator veli palatini muscles which elevates the soft palate against the posterior nasopharyngeal wall. Medial contraction of the lateral pharyngeal wall musculature in combination with slight anterior movement of the posterior pharyngeal wall creates Passavant's ridge, which is a ridge of tissue against which the velum is approximated during the first portion of the pharyngeal phase of swallowing (21, 22).
Following velopharyngeal closure, the first event in the normal swallow sequence, preceding even genioglossus electromyography activity which signals elevation of the hyoid-laryngeal complex, is true vocal fold adduction (23, 24). It is true vocal fold closure that is the primary laryngopharyngeal protective mechanism to prevent aspiration during the swallow (24). Subsequently, false vocal fold adduction, adduction of the aryepiglottic folds and retroversion of the epiglottis take place (25).
Retroversion of the epiglottis, while not the primary mechanism of protecting the airway from laryngeal penetration and aspiration, acts to anatomically direct the food bolus laterally towards the pyriform sinuses. Since the true vocal folds adduct during the swallow, a finite period of apnea must necessarily take place with each swallow. When relating deglutition to respiration, it has been demonstrated that deglutition occurs most often during expiration and includes a period of apnea ranging from 0.3 sec to 2.5 seconds (26, 27). The clinical significance of this finding is that patients with a baseline of compromised lung function will, over a period of time, develop respiratory distress as a meal progresses. This will lead to fatigue during the meal and the consequent risks of laryngeal penetration and aspiration (27). This fact underscores the importance of having available a swallowing evaluation technique that permits observation of patient fatigue.
Following closure of the larynx, pharyngeal peristalsis then takes place by sequential contraction of the superior, middle and inferior pharyngeal constrictor muscles (28). With contraction of the superior pharyngeal constrictor muscle, the laryngeal elevation takes place. The larynx elevates because of the hyoid bone and tongue base moving anteriorly secondary to contraction of the mylohyoid, geniohyoid, stylohyoid and anterior digastric muscles (5). This anterior movement of the larynx combined with the contraction of the middle and inferior constrictor muscles strips the food bolus inferiorly, ushering in the final portion of the pharyngeal phase which is entry of the food bolus into the cervical esophagus.
The duration of the pharyngeal phase of swallowing is about 1 sec. Increasing bolus viscosity has been shown to delay pharyngeal transit, increase the duration of pharyngeal peristaltic waves and prolong and increase upper esophageal sphincter (UES) opening. Increasing bolus volume results in earlier onset of tongue base movement, superior palatal movement, anterior laryngeal movement and UES opening (29). Earlier UES opening results in increased duration of sphincter opening as well as increasing sphincter diameter. Pharyngeal transit time also increases slightly with advancing age. The peristaltic wave sweeping down the pharynx moves along at a rate of approximately 12 cm/sec (29).
While the oral and pharyngeal phases of swallowing are presented sequentially, the physiologic reality is that these phases are integrally related. McConnel described swallowing as a pressure-generation mechanism powered by a two-pump system. He called these pumps the oropharyngeal propulsion pump (OPP) and the hypopharyngeal suction pump (HSP) (30). The OPP is the pressure generated as the anterior two thirds of the tongue propels the food into the oropharynx accompanied by contraction of the pharyngeal constrictor muscles. The HSP is the negative pressure generated as the hyoid-laryngeal complex is elevated away from the posterior pharyngeal wall effectively drawing the food bolus towards the UES. Underscoring the importance of normal tongue mobility for normal deglutition to take place is the fact that any condition that affects the anterior two thirds of the tongue will necessarily affect the OPP and that any problems affecting the tongue base will alter the HSP.
The UES provides a high pressure zone between the pharynx and esophagus remaining closed at rest so as to separate the laryngopharynx from the esophagus. Three muscles contribute to the formation of the UES, the cricopharyngeus muscle, the most inferior muscle fibers of the inferior constrictor muscle and the most superior portion of the longitudinal esophageal muscular fibers (31). These three muscles attach to the posterior lamina of the cricoid cartilage. Just deep to the UES, also along the posterior lamina of the cricoid cartilage, is the posterior cricoarytenoid muscle, the primary abductor of the vocal folds.
At rest, the posterior aspect of the cricoid cartilage rests along the hypopharyngeal wall. Upon elevation of the larynx away from the posterior pharyngeal wall, the post cricoid region separates from its resting position along the posterior hypopharyngeal wall thereby creating a stretching effect upon the UES (32). The cricopharyngeus has a continual basal tone which relaxes during the swallow (33, 34). Studies have shown that UES relaxation takes place during elevation of the hyoid and larynx and reaches its most complete relaxation at the apex of hyoid and laryngeal elevation (35). What is anatomically taking place is that the cricoid cartilage is pulled forward by the motion of the hyoid bone and by contraction of the thyrohyoid muscle. This forward motion of the cricoid snaps open the UES (36). The UES then closes while the larynx is descending to its resting position (37). Of note, the UES exhibits a sustained contraction prior to resuming its basal tone, presumed to assist in preventing immediate regurgitation once the food bolus enters the esophagus (38).
Regarding motor and sensory innervation of the cricopharyngeus, the majority of the work in this area had been on non-human subjects thereby creating significant controversy when applying animal-subject findings to human physiology. Recent work in humans has led to a consensus that the cricopharyngeus receives its motor innervation primarily from the vagus nerve, and to a lesser extent from the glossopharyngeal nerve and from sympathetic nerves through the cranial nerve ganglia (39, 40). The significant sensory contributions to the cricopharyngeus are from the ninth nerve with some contributions from the vagus nerve as well (40, 41, 42).
Esophageal Phase
Like the pharyngeal phase of swallowing , the esophageal phase of swallowing is under involuntary neuromuscular control. However, propagation of the food bolus is significantly slower than in the pharynx with transit time decreasing to 3-4 cm/sec (29). The esophagus connects the pharynx to the stomach and can be divided into three zones (43). The upper zone of the esophagus contains striated muscle beginning at the UES and continuing inferiorly for approximately 6-8 cm where the striated muscle of this zone begins to interdigitate with the smooth muscle of the middle zone, which represents the main portion of the esophagus. The outer fibers of the upper zone are arranged longitudinally while the inner fibers have a circular configuration. Subsequent to relaxation of the cricopharyngeus the primary peristaltic wave of esophageal propagation begins manifested by contraction of the longitudinal muscles followed immediately by contraction of the circular muscle (43). Recent work has demonstrated that the primary peristaltic wave is actually two waves with the first wave dissipating at the end of the upper zone of the esophagus simultaneous with the generation of a second wave which continues to the distal portion of the esophagus (44). This physiologic second wave is likely what has been called secondary esophageal peristalsis which is defined as a reflex response to esophageal distention alone (45).
The middle zone begins where the striated and smooth muscle regions join and extends to within 4 cm of the lower esophageal sphincter (LES). While the upper zone peristaltic wave is under direct central neural control, in the middle zone the peristaltic wave is primarily controlled by the nerves of the myenteric plexus which are located between the outer longitudinal and inner circular muscle layers (46).
The lower zone of the esophagus contains a short segment of smooth muscle esophagus terminating into the LES. The LES is an actual anatomic sphincter with localized muscle changes in the circular muscle (47). Like the UES, the LES is tonically contracted, however, unlike the UES, there is no constant EMG activity in the LES (43). Anatomically contributing to the LES are the diaphragmatic crura which have a sphincteric action during inspiration or straining, which is normally superimposed on the LES (48).
Airway Protective Mechanisms Against Aspiration
The airway protective mechanisms that prevent reflux can be divided into two groups, basal mechanisms and response mechanisms (49). The basal mechanisms operate constantly, typically without need for stimulation, with the LES and UES being the two best examples. The response mechanisms are a series of reflexes that generally require either distension of the esophagus or mechanical stimulation of the pharynx. These reflexes include the esophago-UES reflex (50), the pharyngo-UES reflex, the esophagoglottal closure reflex and the pharyngoglottal closure reflex.
The esophago-UES reflex is a vagally mediated reflex in which distention of the esophagus causes increased UES pressure or increased cricopharyngeal EMG activity. Distention of the proximal esophagus is a stronger stimulus for eliciting this reflex than distention of the distal esophagus (50, 51). The afferent nerve supply to this reflex is from vagal afferents and slow adapting fibers of the muscular wall of the esophagus.
The pharyngo-UES reflex is an experimentally-induced reflex resulting in an increase in resting tone of the UES upon water stimulation of the pharynx (42). The superior laryngeal nerve branch of the vagus is the afferent nerve supply to this reflex with the efferent source the somato-motor nerves from the vagus.
Abrupt distention of esophagus results in the vocal fold adduction of the esophagoglottal closure reflex (52). The afferent supply is the vagus nerve carrying sensory fibers to the brainstem in response to stimulation of stretch receptors in the body of the esophagus. This reflex has been evoked during spontaneous gastroesophageal reflux episodes (53).
Finally, the pharyngoglottal closure reflex is a presumed airway protective reflex which results in brief vocal fold closure upon stimulation of the pharynx with water (54). The afferent and efferent nerve supply is similar to that of the laryngeal adductor reflex with afferent innervation via the internal branch of the superior laryngeal nerve and motor action from the recurrent laryngeal nerve branch of the vagus.
Neural Control of Swallowing
Swallowing is a centrally mediated phenomenon that can be divided into supratentorial and infratentorial regions of control. The supratentorial area of control is located in the frontal cortex anterior to the sensorimotor cortex (55). The infratentorial or brainstem areas involved in control of swallowing are located in the dorsal region within and subjacent to the nucleus of the tractus solitarius as well as in the ventral region around the nucleus ambiguus (56). In both brainstem sites the neurons surrounding the adjacent medullary reticular formation are also involved (57).
In general, the cortical and subcortical regions of the brain are important pathways in the voluntary initiation of swallowing (58, 59). Studies using transcranial magneto-electric stimulation to identify corticofugal projections to the muscles of swallowing have demonstrated that oral muscles, such as the mylohyoid, are represented symmetrically between the two cortical hemispheres, while laryngopharyngeal and esophageal muscles are represented asymmetrically, with most people having a dominant swallowing hemisphere (60). The clinical implication of these findings is that one could expect oropharyngeal dysphagia to result from a unilateral cortical stroke (61).
The brainstem is responsible for the involuntary (pharyngeal and esophageal) phases of swallowing. The dorsal and ventral medullary regions controlling swallowing are represented on both sides of the brainstem and are interconnected. Either side can coordinate the pharyngeal and esophageal stages of deglutition, however because they are interconnected, normal motor and sensory functioning on each side of the laryngopharynx depends on intactness on both sides of the medulla (62, 63). The clinical implication is that a unilateral medullary lesion, say after an embolic stroke, can result in bilateral pharyngeal motor and sensory dysfunction (64, 65).
