AMERICAN JOURNAL OF PHYSIOLOGY

Vol. 221, No. 5, November 1971. Printed in U.S.A.

Role of the pharyngeal plexus in

initiation of swallowing

WILLIAM J. SINCLAIR
Faculty of Dentistry, University of Toronto, Toronto, Canada

SINCLAIR, k%J.JAM J. Role of the pharyngeal pbxus in initiation of colliculus. The preparations were made in a fashion similar
swallowing. Am. J. Physiol. 221(5) : 1260-1263. 1971.-In to those described in a previous study (16). In order to
preparation for stimulation studies, 22 cats were electrolytically differentiate swallowing from other reflex activity, electro-
decerebrated. The intact cephalic branch of the pharyngeal branch myographic recordings were made from mylohyoid, genio-
of the vagus nerve (Za) was electrically stimulated to determine hyoid, and cricothyroid muscles. In addition, changes in
its role in the initiation of the swallowing reflex. Comparative data
intratracheal pressure were monitored by a volumetric pres-
were recorded for the superior laryngeal nerve (SLN) and the
glossopharyngeal nerve (GPN). Swallowing was noted visually sure transducer (Grass PT5) attached to the trachea.
and recorded electromyographically. Stimulation of branch 22a Nerves under investigation were bathed in light paraffin oil
resulted in swallowing in six cases out of 18. Chronaxie and opti- and stimulated intact with bipolar electrodes fitted with a
mum frequency of stimulation for swallowing for branch ,?;?a were polyethylene sleeve. Nerves were excited using a square-
0.11 msec and 30-50 cycles/set, respectively. Afferents for swal- wave stimulator (Grass S4) isolated from ground. In order
lowing were shown to be distributed among pharyngeal branches to avoid shorting through tissue fluid around the nerves, the
of the GPN. Stimulation studies indicated that the GPN is the light paraffin oil was aspirated and replenished every 2 or
primary afferent for swallowing initiated from the pharynx: 3 min. Except in those studies to determine the level of
branch 22a played a minor role. A composite schema is presented excitation reached in the swallow center when branch .?,?a
of those nerves that were found to contain afferents for swallowing.
and the SLN were selectively stimulated, 15 set were
Small and larger sized fibers are suggested as interacting centrally
allowed between successive stimulations in order to prevent
to explain the observation that electrical stimulation of the SLN
elicits swallowing more readily than stimulation of the GPN. central buildup of excitation. The resulting reflex activity
was suitably amplified and photographed on 35-mm paper.
innervation of pharynx; reflex swallowing; pharyngeal reflex The cephalic branch of the pharyngeal branch of the
vagus nerve (Fig. 1, 22a) was investigated in 22 animals
to describe its role in the initiation of reflex swallowing.
Comparative data were also obtained from the SLN and
REFLEX SWALLOWING may be initiated by mechanical or GPN. In selected animals, data were obtained on the role
water stimulation of appropriate sites innervated by the played by the caudal ramus of the GPN which anastomoses
trigeminal (TN), the glossopharyngeal (GPN), and the with the pharyngeal plexus of nerves (Fig. 1, Gpiv 21), the
vagus nerves. Suitable electrical stimulation of the TN (7, small branches of the GPN which form a plexus over the
2 1), the GPN (3, 7, 14, 2 l), the superior laryngeal nerve pharyngeal mucosa (Fig. 1, 19b), the terminal branches of
(SLN) (3, 7, 9, 14, 15, Zl), the recurrent branch (7, 15, the GPN as it arborizes to supply the papillae on the dorsal
Zl), and the accessory recurrent branch (15) of the vagus surface of the base of the tongue (Fig. 1, 19a), the pharyngeal
nerve will also result in swallowing. The SLN is the primary branch of the vagus nerve (Fig. 1, Vagus ZZ), and the caudal
afferent for swallows initiated from the larynx, and the branch of the pharyngeal branch of the vagus nerve (Fig.
GPN serves a similar role for the pharynx. The pharyngeal 1, 22b).
branch of the vagus nerve (designated branch 22 by Stowell) Strength-duration curves and chronaxie determinations
has been reported to play a minor role as an afferent for the were made for the SLN, GPN, and branch 22’a in four
swallowing reflex initiated from the pharynx of the cat (16). animals. Optimum and limiting frequencies were also deter-
The purpose of this study was to investigate the reflex mined for branch 22a. The optimum frequency was assessed
activity resulting from electrical stimulation of the cephalic by the brevity of the latent period to the initiation of the
branch of the pharyngeal branch of the vagus nerve (Za). first swallow as well as the shortest interval encompassing
The other components of the pharyngeal plexus of nerves the initiation of the three successive swallows.
were also explored to determine the role played by each as Branch ZZa and the SLN were selectively stimulated in one
an afferent for the swallowing reflex. animal to evaluate each nerve’s contribution to the level of
excitation in the swallow center. A threshold stimulus to
METHOD the SLN, which resulted in a series of three swallows, was
In preparation for stimulation studies, 22 adult cats were followed by a subthreshold stimulus applied to branch 22a
electrolytically decerebrated at the level of the superior at time intervals of 0, 5, 10, and 20 set after the last re-
1260
SWALLOWING 1261

corded swallow. The procedure was then reversed and a the optimum frequency range. Sporadic swallowing could
subthreshold stimulus was applied to the SLN after thresh- be recorded when branch 22a was stimulated as low as 10
old stimulation of branch 22a. cycles/set and as high as 300 cycles/set. The swallowing
reflex fell off sharply below 15 cycles/set and above 100
cycles/set. The limiting frequencies were therefore deter-
RESULTS
mined to be 15 and 100 cycles/set.
In 18 animals, electrical stimulation of branch Za resulted Electrical stimulation of branch 22b resulted in sporadic
in increased motor activity limited to the superior swallowing activity; the observed increase in motor activity
pharyngeal musculature and a slight change in the depth in this instance was limited to the muscles of the lower
of respiration. Reflex swallowing was noted in addition to pharynx and larynx. In four animals examined, two
the observed motor and respiratory effects in only six showed swallows when branch vagus 22 was stimulated
animals. Marked respiratory reflexes such as coughing were electrically, but all demonstrated increased motor activity
not observed. In two animals, electrical stimulation resulted in the pharynx and larynx.
in respiratory movements similar to sniffing. Electrical stimulation of the SLN at 0.2-0.5 v with
Swallowing initiated by electrical stimulation of branch square pulses of 1 msec duration initiated reflex swallowing
22a at 0.2-9.5 v with square pulses of 1 msec duration was in all 15 animals examined. The average latency to the
characterized by an initial swallow of short latency (1.5 first recorded swallow was 4.0 set and was much longer
set). Sequential swallowing activity could be elicited but than that recorded for branch 22a (1.5 set). The time interval
was not as consistent a finding as for the SLN or the GPN. required to encompass the initiation of three successive
“Afterswallowing” activity was not recorded for branch Za swallows (9.0 set) was approximately the same as that for
when electrical stimulation was terminated. These data branch 22a. Consistently, sequential swallowing activity was
are summarized in Table 1. Electrical stimulation of more readily elicited from the SLN. These data are sum-
branch 2Za at higher voltages (2.6 v) than those required for marized in Table 1. Electrical stimulation of the SLN at
swallowing did not result in marked initial inspirations or higher voltages (2.6 v) than those required for swallowing
coughing so characteristic of the SLN. was characterized by marked initial respiratory reflexes and
The optimum frequency of stimulation of branch 22a for coughing. Limb movements and vomiting were occasion-
swallowing at 0.2-0.5 v with square pulses of 1 msec dura- ally noted.
tion was found to be 30-50 cycles/set. Table 1 summarizes Electrical stimulation of the GPN at 0.5 v with square
the results of stimulation for swallowing within and beyond pulses of 1 msec duration elicited swallowing activity in 12
animals; however, reflex swallowing was evoked with much
greater difficulty than with the SLN or branch Ea. In only
TABLE 1. Results of electrical stimulation of SIN, GpN, and
two animals could no swallowing activity be elicited. When
22a *forswallowing swallowing activity was recorded, the latency to the first
Nerve Branch
swallow and the time to initiate three successive swallows
was much longer than for the SLN or branch 22a (see Table
Braltch Z2a SLN GPN 1). Sequential and afterswallowing activity was a consistent
I I
finding for the GPN. Electrical stimulation of the GPN at
Stimulating frequency
higher voltages (2.6 v) than those required for swallowing
Outside activity was characterized by marked initial respiratory
Optimum optimum Optimum Optimum reflexes often accompanied by limb movements. Occasion-
range, 304 range, 10-2: range, 30-M range, 30-50
cycles/set 55-100 cycles/set cycles/set ally, vomiting or coughing was also recorded.
cycles/set
Electrical stimulation of branch 19a and 19b in the three
No. of nerves tested 6 3 15 12 and five animals examined respectively resulted in swallow-
No. of recorded 41 23 59 30 ing activity in all instances. Stimulation of branch GPN 21
stimulations resulted in swallowing activity in only three of the five
Average latency to 1.5 set 2.0 set 4.0 set 8.5 set animals investigated. The respiratory effects associated with
first recorded
stimulation of these three branches of the GPN were similar
swallow
Range Range Range Range to those recorded for the main trunk of the GPN, except
0.2-6.1 0.2-l 1.1 0.4-l 1.4 0.3-l 7.4 that these effects were less intense and no limb movements
No. of latencies 26 (63% 11 (49% 4 (7%) 3 (10%) or coughing were noted. Figure 1 summarizes the results
under 1 set of the stimulation studies; the shaded areas represent
Average time interval 9.0 set 10.0 set 10.0 set 17.1 set
to initiate 3 probable pathways for the afferent fibers initiating reflex
swallows swallowing.
Range Range Range Range The strength-duration curves for swallowing for the SLN,
2.5-21.2 4.4-18.5 2.2-26.9 6.3-35.6
GPN, and branch 22a are summarized in Fig. 2. Note that
No. of stimulations 20 (50% 16 (70% 56 (95%) 22 (73%)
the threshold for swallowing initiated by electrical stimula-
resulting in 3
swallows tion of the GPN tends to be higher than that of branch 22a
No. of stimulations 7 (44% No data 19 (90%) or the SLN. For a pulse duration of 1 msec, the threshold
resulting in more for swallowing initiated by stimulation of the GPN (0.4 v)
than 3 swallows
is approximately twice that required for branch 22a or the
1262 W. J. SINCLAIR

cat. This supports the findings of previous investigators (3,

7, 14, 2 1). In contrast to the GPN, branch 22a clearly plays
a minor role in the initiation of reflex swallowing from the
pharynx and probably distributes afferents for swallowing
via branch vagus 22. The GPN distributes afferents for
swallowing mainly through branches 19, and IYb and less
frequently via branch GPN 21. Branch 19b L probably innervates
areas coresponding approximately to regions which were
PI. Phar.
found to be most reflexogenic for swallowing when mechan-
ically stimulated (16). With so much sensory overlap, branch
22a would be expected to add sensory support to these same
areas. Since the base of the tongue may (4) or may not (16)
produce swallows when mechanically stimulated, results
reported here for branch 19a may have been due to spread
of excitation to the main trunk of the GPN. Since branch
GPN 21 anastomoses freely with the pharyngeal plexus, it
FIG. 1. A composite schema to show those pharyngeal branches of is possible that branch 22a may distribute afferents for
GPN and vagus nerve which were found to initiate swallowing from swallowing via branch GPN 21 to the main trunk of the
pharyngeal area. X-vagus nerve; IX-glossopharyngeal nerve; GPN. In those instances where the GPN was shown to
SLN-superior laryngeal nerve; Pl. Phar. -pharyngeal plexus; M.
have no swallowing activity, branch 22a would be expected
phar. -motor nerve to pharyngeal musculature; car. -carotid;
Tons. -tonsillar; D-main trunk of GPN proximal to 19b; 19b-small to assume more significance in initiating swallowing from
branches of GPN which form pharyngeal plexus over pharyngeal the pharynx. This may explain why bilateral glossopharyn-
mucosa proximal to 19a; 19a -terminal branches of GPN as it arborizes geal rhyzotomy has no effect on the swallowing reflex (1).
to supply papillae on dorsal surface of base of tongue; GPN Z-caudal The optimum and limiting frequencies for swallowing
ramus of GPN which anastomoses with pharyngeal plexus of nerves;
vagus 22-pharyngeal branch of vagus nerve; ZZa-cephalic branch of found in this study of branch 22a are comparable with
vagus 22; ZZb-caudal branch of vagus 22; 24-pharyngeal ramus of Doty’s (3) findings for the SLN of the cat and indicate their
226. Legend has been taken from Stowell (18, 19). However, prefix probable convergence upon common swallowing half-
GPN has been added to branch 21 and the prefix vagus has been added centers (4).
to branch 22. Designations 19, 19a, and 19b have also been added.
The differences both in the latent periods to the initiation
Shaded areas represent probable pathways of afferent fibers initiating
reflex swallowing. Shading is not suggested to exclude other sensory of the first swallowing reflex and the time interval to include
or motor functions. the initiation of three successive swallows elicited by elec-
trical stimulation of the SLN, GPN, and branch 22a are best
explained by the central effects of the different sensory
afferents excited in each nerve. Pain input has been sug-
gested as masking expected gustatory sensation when the
human SLN was electrically stimulated (11). Also, electrical
stimulation of the central cut end of the SLN after section
of the GPN has been reported as increasing swallowing
activity (20). Since observed latencies to the first swallow
were shortest for branch ZZa, there may be either less central
inhibition to swallowing activity when this nerve is stimu-
lated or more excitation centrally in the swallowing center.
.Ol I I I IllIll I I IIIIIII I IJ
Evidence to reject the latter explanation is shown by the
.Ol .05 , 0.1
MSEC.
0. 2 0.5 1.0 2.0 3.0 40 lack of observed afterswallowing when electrical stimula-
FIG. 2. Strength-duration curves for swallowing initiated by elec- tion of branch 22a was terminated. Also, the swallowing
trical stimulation of SLN, GPN, and branch 22a at 40 cycles/set with reflex was not facilitated when a subthreshold stimulus to
various pulse durations. Approximate chronaxie determinations for the SLN was applied following swallowing activity initiated
SLN, GPN, and branch 22a are 0.08, 0.17, and 0.11 msec, respectively. by threshold stimulation of branch 22a.
Because SLN did facilitate the swallowing reflex, and
SLN (0.2 v). Th e average chronaxie for these nerves was
since both the SLN and GPN often gave afterswallowing
found to be approximately 0.12 msec. activity, both nerves are given larger central representation
Central facilitation studies indicated that swallowing in the swallowing centers than is branch 22a.
only could be initiated by subthreshold stimulation of Whether small or larger sized fibers are chiefly involved
branch 22a when threshold stimulation of the SLN preceded in the swallowing reflex has not been established; both
by less than 10 sec. Subthreshold stimulation of the SLN
medium (6) and larger sized fibers (12, 17) have been
was not effective when applied after swallowing initiated by implicated as afferents for the swallowing reflex. The results
threshold stimulation of branch 22a.
of chronaxie determinations indicate that the afferent fibers
initiating reflex swallowing from the pharynx are probably
DISCUSSION
in the small or medium size range. However, these data
Results of this study indicate that the GPN is the primary must be interpreted with care since histological studies
afferent for swallowing initiated from the pharynx of the describe the SLN (5, 10, 11) and the GPN (2, 22) as ho-
SWALLOWING 1263

mogeneous mixed nerves. The shortness of the latency to the gating for pain must also be considered. Selective blocking
first swallow initiated by electrical stimulation of branch 22a of certain populations of nerve fibers and observing the
and the absence of other reflex activity so typical of the resultant changes in reflex activity may prove successful in
SLN and GPN may indicate that swallowing is initiated by describing more clearly the fiber size serving as the afferent
afferent fibers typified in this nerve. Presently available for the swallowing reflex. Histological analysis of the
data indicate that branch 2’Za is composed of sensory fibers branches Za, Zb, and vagus 22 is underway and may prove
chiefly of the small myelinated type (5). However, little helpful since a knowledge of the caliber spectrum of fibers
data are available on the caliber spectrum of the nerve composing these nerves may also shed some light on the
diameter of the fibers involved in swallowing.
fibers making up branch vagus 22 and its cephalic (22a) or
caudal (22b) ramifications. Since slightly higher voltages The author thanks Dr. A. T. Storey for his advice and encourage-
were required to elicit coughing instead of swallowing ment.
from the SLN and GPN, the nerve fibers serving as afferents This study was supported by Medical Research Council Grant MA
for the cough reflex are probably only slightly smaller than 3584*
Parts of this study were submitted in partial fulfilment of the re-
the afferent fibers initiating the swallowing reflex. However, quirements for a Master of Science in Dentistry at the University of
the interaction of small and larger sized fibers centrally as Toronto.

presented by Melzack and Wall (8) to explain spinal Received for publication 13 January 1971.

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