role of the pharyngeal plexus in initiation of swallowing

8/9/2019 Role of the Pharyngeal Plexus in Initiation of Swallowing

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AMERICAN JOURNAL OF PHYSIOL OGYVol. 221, No. 5, Novemb er 1971. Printed in U.S.A .

Role of the pharyngeal plexus ininitiation of swallowing

WILLIAM J. SINCLAIRFaculty of Dentistry, University of Toronto, Toronto, Canada

SINCLAIR, k%J.JAM J. Role of the pharyngeal pbxus in initiatio n ofswallowing. Am. J. Physiol. 221(5) : 1260-1263. 1971.-Inpreparation for stimulation studies, 22 cats were electrolytical lydecerebrated. The intact cephalic branch of the pharyngeal branchof the vagus nerve (Za) was electrically stimulated to determineits role in the initiation of the swallowing reflex. Comparative datawere recorded for the superior laryngeal nerve (SLN) and theglossopharyngeal nerve (GPN). Swallowing was noted visual lyand recorded electromyographically. Stimulation of branch 22aresulted in swallowing in six cases out of 18. Chronaxie and opti-mum frequency o f stimulation for swallowing for branch ,?;?a were0.11 msec and 30-50 cycles/set, respectively. Afferents for swal-lowing were shown to be distributed among pharyngeal branchesof the GPN. Stimulation studies indicated that the GPN is theprimary afferent for swallowing initiated from the pharynx:branch 22a played a minor role. A composite schema is presentedof those nerves that were found to contain afferents fo r swallowing.Small and larger sized fibers are suggested as interacting centrallyto explain the observation that electrical stimulation of the SLNelicits swallowing more readily than stimulation of the GPN.

innervation of pharynx; reflex swallowing; pharyngeal reflex

REFLEX SWALLOWING may be initiated by mechanical orwater stimulation of appropriate sites innervated by thetrigeminal (TN), the glossopharyngeal (GPN), and thevagus nerves. Suitable electrical stimulation of the TN (7,2 1 , the GPN (3, 7, 14, 2 l), the superior laryngeal nerve(SLN) (3, 7, 9, 14, 15, Zl), the recurrent branch (7, 15,Zl), and the accessory recurrent branch (15) of the vagusnerve will also result in swallowing. The SLN is the primaryafferent for swallows initiated from the larynx, and theGPN serves a similar role for the pharynx. The pharyngealbranch of the vagus nerve (designated branch 22 by Stowell)has been reported to play a minor role as an afferent for theswallowing reflex initiated from the pharynx of the cat (16).The purpose of this study was to investigate the reflexact ivi ty resulting from electrical stimulation of the cephalicbranch of the pharyngeal branch of the vagus nerve (Za).The other components of the pharyngeal plexus of nerveswere also explored to determine the role played by each asan afferent for the swallowing reflex.METHOD

In preparation for stimulation studies, 22 adult cats wereelectro lytically decerebrated at the level of the superior

colliculus. The preparations were made in a fashion similarto those described in a previous study (16). In order todifferentiate swallowing from other reflex act ivi ty, electro-myographic recordings were made from mylohyoid, genio-hyoid, and cricothyroid muscles. In addition, changes inintratracheal pressure were monitored by a volumetric pres-sure transducer (Grass PT5) attached to the trachea.Nerves under investigation were bathed in light paraffin oiland stimulated intact with bipolar electrodes fitted with apolyethylene sleeve. Nerves were excited using a square-wave stimulator (Grass S4) isolated from ground. In orderto avoid shorting through tissue fluid around the nerves, thelight paraff in oil was aspirated and replenished every 2 or3 min. Except in those studies to determine the level ofexcitation reached in the swallow center when branch .?,?aand the SLN were selec tively stimulated, 15 set wereallowed between successive stimulations in order to preventcentral buildup of excitation. The resulting reflex act ivi tywas suitably amplified and photographed on 35-mm paper.

The cephalic branch of the pharyngeal branch of thevagus nerve (Fig. 1, 22a) was investigated in 22 animalsto describe its role in the initiation of reflex swallowing.Comparative data were also obtained from the SLN andGPN. In selected animals, data were obtained on the roleplayed by the caudal ramus of the GPN which anastomoseswith the pharyngeal plexus of nerves (Fig. 1, Gpiv 21), thesmall branches of the GPN which form a plexus over thepharyngeal mucosa (Fig. 1, 19b), the terminal branches ofthe GPN as it arborizes to supply the papillae on the dorsalsurface of the base of the tongue (Fig. 1, 19a), the pharyngealbranch of the vagus nerve (Fig. 1, Vagus ZZ), and the caudalbranch of the pharyngeal branch of the vagus nerve (Fig.1, 22b).

Strength-duration curves and chronaxie determinationswere made for the SLN, GPN, and branch 22a in fouranimals. Optimum and limiting frequencies were also deter-mined for branch 22a. The optimum frequency was assessedby the brev ity of the latent period to the initiation of thefirst swallow as well as the shortest interval encompassingthe initiation of the three successive swallows.

Branch ZZa and the SLN were select ively stimulated in oneanimal to evaluate each nerves contribution to the level ofexcitation in the swallow center. A threshold stimulus tothe SLN, which resulted in a series of three swallows, wasfollowed by a subthreshold stimulus applied to branch 22aat time intervals of 0, 5, 10, and 20 set after the last re-

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SWALLOWING

corded swallow. The procedure was then reversed and asubthreshold stimulus was applied to the SLN after thresh-old stimulation of branch 22a.

RESULTSIn 18 animals, electrical stimulation of branch Za resulted

in increased motor act ivi ty limited to the superiorpharyngeal musculature and a slight change in the depthof respiration. Reflex swallowing was noted in addition tothe observed motor and respiratory eff ect s in only sixanimals. Marked respiratory reflexes such as coughing werenot observed. In two animals, electrical stimulation resultedin respiratory movements similar to sniffing .

Swallowing initiated by electrical stimulation of branch22a at 0.2-9.5 v with square pulses o f 1 msec duration wascharacterized by an initial swallow of short latency (1.5set). Sequential swallowing act ivi ty could be elicited butwas not as consistent a finding as for the SLN or the GPN.Afterswallowing act ivi ty was not recorded for branch Zawhen electrical stimulation was terminated. These dataare summarized in Table 1. Electrical stimulation ofbranch 2Za at higher voltages (2.6 v) than those required forswallowing did not result in marked initial inspirations orcoughing so characteristic of the SLN.

The optimum frequency of stimulation of branch 22a forswallowing at 0.2-0.5 v with square pulses of 1 msec dura-tion was found to be 30-50 cycles/set. Table 1 summarizesthe results of stimulation for swallowing within and beyond

TABLE 1. Results of electrical stimulation of SIN, GpN, and22a *forswallowing

No. of nerves testedNo. of recorded

stimulationsAverage latency to

first recordedswallow

No. of latenciesunder 1 set

Average time intervalto initiate 3swallows

No. of stimulationsresulting in 3swallows

No. of stimulationsresulting in morethan 3 swallows

Nerve BranchBraltch Z2a SLN GPNI I

Stimulating frequency

Optimumrange, 304cycles/set

641

1.5 set

Range0.2-6.1

26 (63%9.0 set

Range2.5-21.2

20 (50%

Outsideoptimumrange, 10-2:55-100cycles/setOptimumrange, 30-Mcycles/set

Optimumrange, 30-50cycles/set

323

2.0 set

15594.0 set

1230

8.5 set

Range Range Range0.2-l 1.1 0.4-l 1.4 0.3-l 7.4

11 (49% 4 (7%) 3 (10%)10.0 set 10.0 set 17.1 set

Range Range Range4.4-18.5 2.2-26.9 6.3-35.616 (70% 56 (95%) 22 (73%)

7 (44% No data 19 (90%)

1261the optimum frequency range. Sporadic swallowing couldbe recorded when branch 22a was stimulated as low as 10cycles/set and as high as 300 cycles/set. The swallowingreflex fell of f sharply below 15 cycles/set and above 100cycles/set. The limiting frequencies were therefore deter-mined to be 15 and 100 cycles/set.

Electrical stimulation of branch 22b resulted in sporadicswallowing act ivi ty; the observed increase in motor act ivi tyin this instance was limited to the muscles of the lowerpharynx and larynx. In four animals examined, twoshowed swallows when branch vagus 22 was stimulatedelectrica lly, but all demonstrated increased motor act ivi tyin the pharynx and larynx.

Electrical stimulation of the SLN at 0.2-0.5 v withsquare pulses of 1 msec duration initiated reflex swallowingin all 15 animals examined. The average latency to thefirs t recorded swallow was 4.0 set and was much longerthan that recorded for branch 22a (1.5 set). The time intervalrequired to encompass the initiation of three success iveswallows (9.0 set) was approximately the same as that forbranch 22a. Consistently, sequential swallowing act ivi ty wasmore readily elicited from the SLN. These data are sum-marized in Table 1. Electrical stimulation of the SLN athigher voltages (2.6 v) than those required for swallowingwas characterized by marked initial respiratory reflexes andcoughing. Limb movements and vomiting were occasion-ally noted.

Electrical stimulation of the GPN at 0.5 v with squarepulses of 1 msec duration elicited swallowing act ivi ty in 12animals; however, reflex swallowing was evoked with muchgreater dif ficul ty than with the SLN or branch Ea. In onlytwo animals could no swallowing act ivi ty be elicited. Whenswallowing act ivi ty was recorded, the latency to the firstswallow and the time to initiate three success ive swallowswas much longer than for the SLN or branch 22a (see Table1). Sequential and afterswallowing act ivi ty was a consistentfinding for the GPN. Electrical stimulation of the GPN athigher voltages (2.6 v) than those required for swallowingact ivi ty was characterized by marked initial respiratoryreflexes often accompanied by limb movements. Occasion-ally , vomiting or coughing was also recorded.

Electrical stimulation of branch 19a and 19b in the threeand fi ve animals examined respectively resulted in swallow-ing act ivi ty in all instances. Stimulation of branch GPN 21resulted in swallowing act ivi ty in only three of the fi veanimals investigated. The respiratory eff ect s associated withstimulation of these three branches of the GPN were similarto those recorded for the main trunk of the GPN, exceptthat these ef fec ts were less intense and no limb movementsor coughing were noted. Figure 1 summarizes the resultsof the stimulation studies; the shaded areas representprobable pathways for the afferent fibers initiating reflexswallowing.

The strength-duration curves for swallowing for the SLN,GPN, and branch 22a are summarized in Fig. 2. Note thatthe threshold for swallowing initiated by electrical stimula-tion of the GPN tends to be higher than that of branch 22aor the SLN. For a pulse duration of 1 msec, the thresholdfor swallowing initiated by stimulation of the GPN (0.4 v)is approximately twice that required for branch 22a or the


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1262 W. J. SINCLAIR

PI. Phar.

F IG. 1. A composite schema to show those pharyngeal branches ofGPN and vagus nerve which were found to initiate swa llowing frompharyngeal area. X-vagus nerve; IX-glossop haryngeal nerve;SLN-superior laryngeal nerve; Pl. Phar. -pharyngeal plexus; M.phar. -motor nerve to pharyngeal mus culature; car. -carotid;Ton s. -tonsillar; D-main trunk of GPN proximal to 19b; 19b-smallbranche s of GPN which form pharyngeal plexus over pharyngealmucosa proximal to 19a; 19a -terminal branches of GPN as it arborizesto supply papillae on dorsal surface of base of tongue; GPN Z-caudalramus of GPN which a nastomoses with pharyngeal plexus of nerves;vagus 22-pharyngeal branch of vagus nerve; ZZa-cep halic branch ofvagus 22; ZZb-caudal branch of vagus 22; 24-pharyngeal ramus of226. Legend has been taken from Stowell (18, 19). However, prefixGPN has been added to branch 21 and the prefix vagus has been addedto branch 22. Designations 19, 19a, and 19b have also been added.Shaded areas represent probable pathways of afferent fibers initiatin greflex swallowing. Shading is not suggested to exclude other sensoryor motor functions.

.Ol I I I IllIll I I IIIIIII I IJ.Ol .05 , 0.1 0. 2 0.5 1.0 2.0 3.0 40MSEC.

F IG. 2. Strength-duration curves for swallo wing initiated by elec-trical stimulation of SLN, GPN, and branch 22a at 40 cycles/set withvarious pulse durations. Approximate chronaxie determ inations forSLN, GPN, and branch 22a are 0.08, 0.17, and 0.11 msec, respectively.SLN (0.2 v). Th e average chronaxie for these nerves wasfound to be approximately 0.12 msec.

Central facilitation studies indicated that swallowingonly could be initiated by subthreshold stimulation ofbranch 22a when threshold stimulation of the SLN precededby less than 10 sec. Subthreshold stimulation of the SLNwas not eff ect ive when applied after swallowing initiated bythreshold stimulation of branch 22a.DISCUSSION

Results of this study indicate that the GPN is the primaryafferent f or swallowing initiated from the pharynx of the

cat. This supports the findings of previous investigators (3,7, 14, 2 1). In contrast to the GPN, branch 22a clearly playsa minor role in the initiation of reflex swallowing from thepharynx and probably distributes afferents for swallowingvia branch vagus 22. The GPN distributes afferents forswallowing main ly through branches 19, and IYb and lessfrequently via branch GPN 21. Branch 19b probably innervatesLareas coresponding approximately to regions which werefound to be most reflexogenic for swallowing when mechan-ically stimulated (16). With so much sensory overlap, branch22a would be expected to add sensory support to these sameareas. Since the base of the tongue may (4) or may not (16)produce swallows when mechanically stimulated, resultsreported here for branch 19a may have been due to spreadof excitation to the main trunk of the GPN. Since branchGPN 21 anastomoses freely with the pharyngeal plexus, itis possible that branch 22a may distribute afferents forswallowing via branch GPN 21 to the main trunk of theGPN. In those instances where the GPN was shown tohave no swallowing act ivi ty, branch 22a would be expectedto assume more significance in initiating swallowing fromthe pharynx. This may explain why bilateral glossopharyn-geal rhyzotomy has no ef fect on the swallowing reflex (1).

The optimum and limiting frequencies for swallowingfound in this study of branch 22a are comparable withDoty s (3) findings for the SLN of the cat and indicate theirprobable convergence upon common swallowing half -centers (4).

The dif ferences both in the latent periods to the initiationof the first swallowing reflex and the time interval to includethe initiation of three success ive swallows elicited by elec-trical stimulation of the SLN, GPN, and branch 22a are bestexplained by the central effe cts of the different sensoryafferents excited in each nerve. Pain input has been sug-gested as masking expected gustatory sensation when thehuman SLN was electrically stimulated (11). Also, electricalstimulation of the central cut end of the SLN after sectionof the GPN has been reported as increasing swallowingact ivi ty (20). Since observed latencies to the fir st swallowwere shortest for branch ZZa, there may be either less centralinhibition to swallowing act ivi ty when th is nerve is stimu-lated or more excitation centrally in the swallowing center.Evidence to reject the latter explanation is shown by thelack of observed afterswallowing when electrical stimula-tion of branch 22a was terminated. Also, the swallowingreflex was not facilitated when a subthreshold stimulus tothe SLN was applied following swallowing act ivi ty initiatedby threshold stimulation of branch 22a.

Because SLN did facilitate the swallowing reflex, andsince both the SLN and GPN often gave afterswallowingact ivi ty, both nerves are given larger central representationin the swallowing centers than is branch 22a.

Whether small or larger sized fibers are chie fly involvedin the swallowing reflex has not been established; bothmedium (6) and larger sized fibers (12, 17) have beenimplicated as afferents for the swallowing reflex. The resultsof chronaxie determinations indicate that the afferent fibersinitiating reflex swallowing from the pharynx are probablyin the small or medium size range. However, these datamust be interpreted with care since histological studiesdescribe the SLN (5, 10, 11) and the GPN (2, 22) as ho-


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SWALLOWING 1263mogeneous mixed nerves. The shortness of the latency to thefir st swallow initiated by electrical stimulation of branch 22aand the absence of other reflex acti vity so typical of theSLN and GPN may indicate that swallowing is initiated byafferent fibers typified in this nerve. Presently available

gating for pain must also be considered. Selective blockingof certain populations of nerve fibers and observing theresultant changes in reflex activi ty may prove successful indescribing more clearly the fiber size serving as the afferentfor the swallowing reflex. Histological analysis of the

data indicate that branch 2Za is composed of sensory fibers branches Za, Zb, and vagus 22 is underway and may provechiefl y of the small myelinated type (5). However, little helpful since a knowledge of the caliber spectrum of fibersdata are available on the caliber spectrum of the nerve composing these nerves may also shed some light on thefibers making up branch vagus 22 and its cephalic (22a) or diameter of the fibers involved in swallowing.caudal (22b) ramifications. Since slightly higher voltageswere required to elicit coughing instead of swallowing The author thanks Dr. A. T. Storey for his advice and encourage-ment.from the SLN and GPN, the nerve fibers serving as afferents This study was supported by Medical Research Council Grant MAfor the cough reflex are probably only slight ly smaller than 3584*the afferent fibers initiating the swallowing reflex. However, Parts of this study were subm itted in partial fulfilme nt of the re-quirements for a Master of Scie nce in Dentistry at the University ofthe interaction of small and larger sized fibers centrally as Toronto.presented by Melzack and Wall (8) to explain spinal Received for public ation 13 January 1971.REFERENCES

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2. BLOM, S. Afferent influences on tongue musc le activity. A morpho-logical and physiological study in the cat. Acta Physiol. Stand. 49,Suppl. 170:1-97, 1960.

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7. KAHN, R. H. Studien iiber den Schluckreflex. Arch. Physiol. Suppl.27: 386-426, 1903.8. MELZACK, R., AND P. D. WALL. Pain m echanisms: a new theory.

Science 150: 971-979, 1965.9. MILLER, F. R., AND C. S. SHERRINGT ON. Some observations onthe buccopha ryngeal stage of reflex deglutition in the cat. Quart.J. Exptl. Physiol. 9: 147-186, 1916.

10. ODACHI, R. Studien und Untersuch ungen iiber die Urspriinge derKehlkopfnervenfasern. Japan . J. Med. Sc i. Anat. 6 : 153-206, 1936.

11. OGURA, J. H., and R. L. LAM. Anatomical and physiological

correlation s on stim ulation of the human superior laryngeal nerve.Lary ngosc ope 63 : 947-959, 1953.12. POLIKAR POVA, G. A. A note on pharyngeal innervation. Arkh.Anat. Gistol. Embriol. 34: 62-67, 1957.

13. POMMERENKE, W. T. A study of the sensory areas eliciting theswallowing reflex. Am. J. Physiol. 84: 36-41, 1928.

14. PRIIMA, G. YA. The Role of the Superior Laryngeal Nerve in the Regula-tion of Deglutition. Stalingrad : A. S. Serafimovich MunicipalPedagogical Institute, p. 226, 1958.

15. RYLANT, P. Le controle r&lexe de la respiration par les fibressen sible s du nerf recurrent. Arch. Intern. Ph ysiol. 53 : 181-224, 1943.16. SINCLAIR, W. J. Initiation of reflex sw allowing from the naso- andoropharynx. Am. J. Phys iol. 218 : 956-960, 1970.17. STOREY, A. T. A functional analysis of sensory units innervatingepiglo ttis and larynx. Exptl. Neural. 20: 366-383, 1968.

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19. STOWELL, T. B. The glossopharyngeal nerve in the domestic cat.Proc. Am. Phil. Sot. 25 : 90-94, 1888.20. TEITELBAUM , H. A., AND F. A. RIES. A study of the comparativephysiology of the glossopha ryngeal nerve-respiratory reflex in therabbit, cat, and dog. Am. J. Physiol. 112: 684-689, 1935.

21. WALLER, A., AND J. L. PROVOST. Etude relative aux nerfs sensitifsqui president aux ph&om&nes &flexes de la deglutition. Arch.Phys iol. Norm. Pathol. 3 : 185-197 and 343-354, 1870.

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role of the pharyngeal plexus in initiation of swallowing

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