AMERICAN JOURNAL OF PHYSIOLOGY

Vol. 218, No. 4, April 1970. Printed in U.S.A.

Initiation of reflex swallowing from

the naso- and oropharynx

WILLIAM J. SINCLAIR

Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada

SINCLAIR, WILLIAM J. Initiation of rejlex swallowing from the naso- and oropharynx. Am. J. Physiol. 218(4) : 956-960. 1970.~In 15 electrolytically decerebrated cats, the pharynx was exposed surgically from the ventral aspect and divided in the midline. The pharynx was mechanically stimulated with light pressure using a wooden applicator 4 mm in diameter. Swallowing was noted visually and later verified electromyographically. Areas eliciting swallows which occurred within l-3 set after application of the stimulus were recorded on a map of the pharynx. Observations were made on the effects of surface area stimulated, pressure, and movement patterns. The results showed that the posterior pillars were most reflexogenic, the posterior pharyngeal wall was slightly less, and the lateral pharyngeal wall was least reflexogenic. These areas extended into the nasopharynx. Larger diameter probes and heavier pressures appeared to be no more effective. Movement made mechanical stimulation more effective and showed direc- tional sensitivity. Selective sectioning of the glossopharyngeal nerve (GPN) and the pharyngeal branch of the vagus nerve (PhX) demonstrated that the GPN is the prime afferent of the swallow reflex initiated from the pharynx and that the PhX plays a minor role.

reflexogenic sites; innervation of pharynx ; adequate stimulus; pharyngeal reflex

REFLEX SWALLOWING IS A COMPLEX, unconditioned reflex. The intrinsic muscles of swallowing participate in a charac- teristic pattern (4) which can be differentiated from gagging, coughing, and vomiting ( 13). Reflex swallowing is initiated by mechanical or water stimulation of appropriate sites in- nervated by cranial nerves V, IX, and X. Mechanical stim- ulation of the lips ( lo), nasopharynx ( 12, 27), posterior pharyngeal wall (12, 16, 20, 27), soft palate (12, 16, 21, 27), faucial pillars ( 12, 16, 20, 27), dorsum of the tongue ( 16, Zl), pharyngeal surface of the epiglottis (12, 16, 21, 27), and the glossoepiglottideal sinuses ( 16), has been shown to be an adequate stimulus. Water stimulation of the base of the tongue and glossoepiglottideal sinuses ( IS), as well as the glottis and epiglottis (23), was also effective. Cranial nerves V ( 10, 12, 27), IX (3, 12, 21, 27), the superior laryngeal nerve (SLN) (3, 12, 2 1, 27), the recurrent branch of X ( 12, 22, 27), the accessory recurrent branch of X (ZZ), and the main trunk of X (21) have been reported as afferents for the swallowing reflex.

Mechanical stimulation is the most effective stimulus in initiating reflex swallowing from the pharyngeal areas and water or hypotonic solutions from the larynx. Although the SLN is the primary afferent nerve for swallows initiated from

the laryngeal portion of the airway, the role played by the GPN and the trigeminal nerve (TN) shows considerable species variability. In the cat, the GPN ( 12, 27) is described as the primary afferent of the swallow initiated from the pharynx while the TN has little ( 12) or no (27) importance. The paradox that electrical stimulation of the SLN elicits reflex deglutition more readily than does stimulation of the GPN remains unexplained (6). Some human clinical evi- dence ( 1,7, 17) suggests that nerves other than the GPN may be involved in swallowing initiated from the pharynx. The pharyngeal areas initiating swallowing needed to be more carefully examined and the cranial nerve (or nerves) serving these areas more precisely identified. This study was de- signed to map the various pharyngeal areas in the cat as to the relative effectiveness of mechanical stimulation in eliciting swallowing. Some observations were made on the extent and depth of receptor fields, the significance of surface area stimulated, and movement patterns of the stimulus. The relative importance of the GPN and PhX as afferent nerves of the swallow was investigated by selective unilateral sectioning.

METHOD

In preparation for stimulation studies, 15 cats were elec- trolytically decerebrated. After initial anesthetization by intrathoracic administration of 4 % sodium thiamylal (Surital) solution (0.5 ml/kg), the animal was maintained on 4 % Surital solution administered intravenously (0.1 ml as required) while a tracheotomy and craniotomy were per- formed. Coordinates for the decerebration (A5, & 5 mm) were according to the atlas of Jasper and Ajrnone-Marsan ( 11). Atropine sulfate was administered intramuscularly (2 mg/kg) to control oral and airway secretions. The pharynx was exposed from the ventral aspect, divided in the midline, and laid open with springs.

The posterior and lateral pharyngeal walls and the pos- terior pillars were stimulated by applying light pressure with a wooden applicator 4 mm in diameter. In each case the success or failure of a swallow to occur within l-3 set after the application of the stimulus was recorded on a diagram of the pharynx. Motor responses were noted visually and monitored electromyographically. Two unipolar electrodes of .0063-inch enamel-Nichrome wire (Driver Harris) were inserted by means of 26-gauge hypodermic needles into each unilateral mylohyoid, geniohyoid, cricothyroid, and thy- roarytenoid muscle after a technique described by Inman. (The barbed wire electrodes were developed by Prosthetic

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SWALLOWING

Devices Research Project (now Biomechanics Laboratory) at the University of California, Berkeley and San Francisco, during studies of human locomotion.) Electrode placement in the thyroarytenoid muscle was verified surgically at the end of the experiment. Muscle action potentials were dis- played on a Tektronix four-channel cathode-ray oscillo- scope and photographed. The mylohyoid muscle was also monitored on a loud speaker. Figure 1 shows typical recordings of swallowing, glottic closure, sniffing, and coughing. Swallowing was identified by sequential activity in the mylohyoid, geniohyoid, cricothyroid, and thyroary- tenoid muscles. Glottic closure was indicated by a sudden burst of activity in the thyroarytenoid muscle only. Sniffing was shown by an increase in single-unit activity in the thy- roarytenoid muscle. Coughing was characterized by syn- chronous activity in the cricothyroid and thyroarytenoid muscles and an absence of motor activity in the geniohyoid and mylohyoid muscles. An interval of 15 set was allowed between successive stimulaiions to avoid receptor adaptation and central facilitation.

Observations were made on the effects of surface area stimulated by using wooden applicators 1, 2, 3, 5, and 6 mm in diameter. The effects of pressure increases of l-3 oz were investigated using an adapted orthodontic Richmond strain gauge. The effects of movement patterns were observed using the 4-mm probe. After initial contact with the pos- terior pharyngeal wall, the 4-mm probe was slid towards the nasopharynx or larynx to see if there was any directional

957

sensitivity. Finally, the SLN, GPN, and PhX were dissected free of attached fascia and bathed in light liquid paraffin oil. Each nerve was stimulated with a Grass square-wave stim- ulator isolated from ground in order to record typical reflex activity. In ,order, the SLN, GPN, and PhX were sequen- tially sectioned unilaterally. In each instance, the effect on reflex swallowing initiated by mechanical stimulation of the ipsilateral pharyngeal wall was observed.

RESULTS

The results are summarized in Fig. 2. The data show that the most reflexogenic site was located lateral to the posterior pharyngeal wall in an area corresponding to the posterior pillars. In a total of 131 stimulations of this area, 87 % elicited reflex swallowing. The posterior pharyngeal wall was slightly less effective. In a total of 178 stimulations, 80 % produced swallowing. Note that these two areas extended into the nasopharynx for a short distance (l-2 mm). The lateral pharyngeal wall was least effective; only 56 % were successful in 92 stimulations. Observations indicated that only sporadic swallows could be elicited from the peritonsil- lar area and pharyngeal mucosa located close to the vocal cords. The base of the tongue, oro- and nasopharyngeal sur- face of the soft palate (apart from that area included in Fig. 2), and the vocal cords did not give rise to swallowing. Mechanical stimulation of deeper nasopharyngeal tissue resulted in respiratory movements similar to sniffing. Me-

FIG. 1. A: typical electromyographic re- cordings of a swallow initiated by mechanicai stimulation of posterior pharyngeal wall with a probe 4 mm in diameter. B: represents a re- cording of glottic closure on mechanical stimu- lation of vocal cords. C: a recording of respira- tory activity similar to sniffing on mechanical stimulation of deep nasopharyngeal mucosa. D: a recording of a cough due to mechanical stimulation of vocal cords. Horizontal calibra- tion represents 0.5 set, and vertical calibration 500 pv. Mylohyoid = mh; geniohyoid = gh; cricothyroid = ct; and thyroarytenoid muscles = ta.

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958 W. J. SINCLAIR

PP

MODERATE REFLEXOGENIC AREA

FIG. 2. Regions of oro- and nasopharynx from which swallowing was initiated by mechanical stimulation with a probe 4 mm in cross section. Area corresponding to posterior pillars was most effective, posterior pharyngeal wall was slightly less effective, and lateral pharyn- geal wall was least effective. Note that these regions extend onto roof of nasopharynx. Swallowing was only sporadically elicited from periton- sillar areas and pharyngeal mucosa closer to vocal cords. Mechanical stimulation of base of tongue, soft palate, and vocal cords did not elicit swallowing. VC = vocal cords; PP = posterior pillars; LPW = lateral pharyngeal wall; NP = nasopharynx; SP = soft sillar area; PPW = posterior pharyngeal wall.

palate ; PT = periton-

chanical stimulation with a stimulator 4 mm in diameter appeared to be more effective than an applicator of smaller diameter; increasing the surface area of the probe to 5 or 6 mm did not make the probe more effective. Increasing the pressure applied by the 4-mm probe from light pressure to 1, 2, or 3 oz appeared to elicit swallows less readily and sometimes resulted in a cough. In contrast, movement pat- terns did enhance the response. When initial contact of the posterior pharyngeal wall failed to elicit a swallow, sliding the 4-mm probe toward the larynx would occasionally be effective. However, swallows would occur more readily if the probe was slid toward the nasopharynx. By continuing this movement pattern, a series of 4-5 swallows could be elicited.

Figure 3 shows typical reflex activity. The PhX was char- acterized by an initial swallow of short latency (1-2 set) sometimes followed by sequential swallows. The SLN was characterized by an initial swallow of longer latency (3-4 set) followed by sequential swallows. The GPN elicited swallows with greater difficulty; stimulation was often as- sociated with limb and increased respiratory movement. A swallow often occurred when the stimulation was termi- nated.

In 12 decerebrate cats studied, section of the SLN had no effect on swallowing initiated from the ipsilateral pharyngeal wall when mechanically stimulated. Selective section of the

GPN abolished reflex swallowing completely in five animals and partially in four animals. In these four animals, section of the PhX abolished the swallowing reflex. In contrast, sec- tion of the PhX abolished reflex swallowing completely in only two animals. Swallows in all instances could still be elicited from the intact side of the pharynx. It was difficult to describe any specific area innervated by the GPN or the PhX because of their apparent sensory overlap. However, sectioning of the GPN had less effect on swallowing elicited from the dorsolateral aspect of the nasopharynx.

DISCUSSION

The reaexogenic areas mapped in this study amplify previous findings ( 12, 16, 20, 2 1, 27). The surgical prep- aration allowed for closer inspection of the areas stimulated and for the electromyographic identification of the response elicited. The boundaries defined in this study permit com- parison with the fields of single sensory units of the GPN and PhX currently being studied. In this way, the relative role of the GPN and PhX in reflex swallowing can be assessed. The localization of tactile units would be expected to corres- pond to the areas mapped in this study.

The protective role of the swallow in sealing off the naso- pharyngeal isthmus to prevent the influx of material during swallowing has been described. Frenckner (9), from X-ray cinematographic studies, showed that the soft palate in the human is raised against the nasopharyngeal tissue before the base of the tongue contacts the posterior pharyngeal wall. Negus ( 18) and Bosma (2) also support this view. Electro- myographic findings of Doty and Bosma (4) indicate that the palatopharyngeus muscle participates in the lead com- plex. The nasopharyngeal sites mapped in this study would correspond to areas that would be stimulated initially when the soft palate is raised against the posterior pharyngeal wall. Since careful stimulation of the soft palate and the base of the tongue did not produce reflex swallowing, their contact against contiguous structures seems essential to elicit swal- lowing. Movement of the stimulus toward the nasopharynx was more effective than similar movements toward the larynx. The motion of the tongue during deglutition would facilitate swallowing. Clearly swallowing, apart from its classical visceral function, also plays an important protective role in guarding both the nasal and laryngeal portions of the airway.

Some evidence for spatial summation is shown by the greater effectiveness of the larger sized probes. Storey (24) reported that the frequency and adaptation rates for water and tactile units in the larynx were similar. Doty (3) showed that the optimum frequency of stimulation of 30 cycles/set for swallow initiated by electrical stimulation of the SLN was independent of the pattern of the stimulus. Obser- vations reported here would suggest that the surface area stimulated and the sequence of receptor stimulation may hold the key for explaining the mechanism of eliciting reflex swallowing. There is no evidence to suggest that the “pluri- potential” laryngeal receptors described by Storey (24) exist in the pharynx of the cat. Water dropped into the pharynx would not elicit reflex swallowing unless it was allowed to contact the vocal cords or epiglottis. Although mechanical stimulation of the pharynx failed to produce coughing, gag-

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SWALLOWING 959

PhX

A mh

gh

SLN

B mh

FIG. 3. A: typical recorded swallow activity due to electrical stimulation of PhX at 30 cycles/set and 0.4 v. Note that latency to on- set of first swallow is 0.3 set; interval to onset of second swallow is 0.4 sec. Continued stimu- lation failed to produce further swallows. B: typical recorded swallow activity due to elec-

1 1, m trical stimulation of the SLN at 30 cycles/set 1, -- LLLiLLL&LLLL&*~L and 0.2 v. Note that latency to onset of first

swallow is 2.5 set; intervals to onset of succes- sive swallows are 2.2 and 1.1 sec. Two seconds of tracing have been removed before first and second swallow. Arrow indicates onset of stim-

2 SECONDS

ulation. Horizontal calibration represents 0.5 set and vertical calibration 500 E.CV. Mylohy- oid = mh; geniohyoid = gh; cricothyroid E= ct; and thyroarytenoid muscles = ta.

ging, or vomiting, no other stimulus parameters were in- vestigated except for the incidental observations on the effects of water. The effects of two smaller sized probes ap- plied simultaneously in order to determine whether spatial summation occurred were not investigated.

Since heavier pressure of l-3 oz did not enhance the re- sponse, the receptors responsible for reflex swallowing are most likely superficially located. Studies by Miller and Sherrington ( 16) and Pommerenke (20) also support this view. However, Pommerenke (20) found heavier pressures more effective when applied to the posterior pharyngeal wall; in the human the pharyngeal receptors responsible for swallowing appear to be both superficial and deeper seated. From histological studies by Konkin (14) and Polikarpova ( 19) one could implicate the more superficial layers of the mucosa as being the most likely site for the receptors trig- gering swallowing. The occasional cough and increased respiratory movements recorded in this study upon appli- cation of heavier pressures were probably due to the manip- ulation of the main trunk of the GPN rather than due to stimulation of deeper-seated receptors. A similar explana- tion is plausible for the respiratory effects reported by Takagi et al. (25), since respiratory effects are quite com-

mon when the GPN is electrically stimulated (3, 2 1, 26, 27).

Selective sectioning studies indicate that the GPN is the

primary afferent nerve for the swallow initiated from the

pharynx of the cat. These findings support investigations by

Waller and Prevost (27) and Kahn ( 12). Degeneration

studies by Polikarpove ( 19) also indicate that the GPN is a

major source of innervation to the pharyngeal region. This

study suggests that the PhX usually plays a minor role in the

initiation of initiated from GPN and the swallowing in

Preliminary

1 reflex swallowing. Since reflex swallowing the pharynx was abolished by section of the PhX, the TN has little or no significance in the cat. studies indicate that the optimum frequency

of stimulation for the PhX is 50-30 cycles/set; this is similar to Doty’s (3) findings for electrical stimulation of the SLN of the cat. These findings indicate the probable convergence of the SLN and PhX upon a common-swallow half-center described by Doty, Richmond, and Storey (5). Preliminary data indicate that electrical stimulation of the PhX results in swallows of much shorter latency than with stimulation of the SLN. Swallows could also occur without being accom- panied by other reflex activity so characteristic of the GPN and SLN. This may indicate that swallowing is initiated by

the excitation of a fairly homogeneous population of nerve

fibers. Presently available data indicate that larger-sized

fibers (24) or smaller fibers (8) alone may be responsible for

swallowing. Perhaps large and small fibers may interact

centrally in a fashion similar to that postulated by Melzack

and Wall ( 15) to explain spinal gating for pain. This could

account for the paradox that electrical stimulation of the

SLN elicits reflex swallowing more readily than does stim-

ulation of the GPN.

The author is indebted to Dr. A. T. Storey for his valued counsel and encouragement.

This study was submitted in partial fulfilment of the requirements for the Diploma Course in Orthodontics and was supported in part by National Research Council Grant DA- 147.

Received for publication 9 October 1969.

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960 W. J. SINCLAIR

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