Vol. 282, Issue 5, R1342-R1347, May 2002
Pharyngeal branch of the glossopharyngeal nerve plays a major
role in reflex swallowing from the pharynx
Jun-Ichi
Kitagawa,
Tomio
Shingai,
Yoshihiro
Takahashi, and
Yoshiaki
Yamada
Department of Oral Physiology, Niigata University Faculty
of Dentistry, Niigata 951 - 8514, Japan
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ABSTRACT |
Mechanical stimulation of the
pharyngeal areas readily elicits reflex swallowing. However, it
is much more difficult for electrical stimulation of the
glossopharyngeal nerve (GPN) to evoke reflex swallowing than it is for
stimulation of the superior laryngeal nerve (SLN) to do so. These
paradoxical findings remain unexplained; hence, the main purpose of
this study was to explain this contradiction by using a
urethane-anesthetized rat. Mechanical stimulation easily elicited
reflex swallowing from the pharynx. The posterior pillars, posterior
pharyngeal wall, and the soft palate of the rat were extremely
reflexogenic areas for swallowing. Sectioning the pharyngeal branch of
the GPN (GPN-ph), however, eliminated the swallowing reflex from these
areas. In contrast, sectioning the lingual branch of the GPN had no
effect on the elicitation of swallowing. Electrical stimulation of the
GPN-ph and SLN elicited sequentially occurring swallows. The
relationship between stimulus frequency and the latency of swallowing
for the GPN-ph was approximately the same as that for the SLN. These
results indicate that the GPN-ph plays a major role in the initiation
of reflex swallowing from the pharynx in rats.
superior laryngeal nerve; pharyngeal reflex; deglutition; pharyngeal plexus
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INTRODUCTION |
IT IS WELL KNOWN THAT
REFLEX swallowing is mostly elicited from specific areas of the
pharynx and larynx (see reviews in Refs. 3,
5, 13, 14). The
receptive regions eliciting reflex swallowing have been analyzed with
mechanical and chemical stimulation (4, 15, 17, 19-21,
26). In the pharyngeal region, mechanical stimulation is
effective in evoking swallowing. The posterior pillars are the regions
that are the most reflexogenic to mechanical stimulation in the cat
(21). The posterior pharyngeal wall is slightly less
reflexogenic. The receptive regions for swallowing in humans are
essentially similar to those in animals (17). In addition,
in the laryngeal regions, Storey (23, 24) has demonstrated
that water stimulation, as well as mechanical stimulation, is effective
in evoking swallowing. This finding has been confirmed by several
studies (9, 10, 12, 18-20).
The pharyngolaryngeal regions that evoke swallowing are innervated by
the glossopharyngeal nerve (GPN), the pharyngeal branch of the vagus
nerve (X-ph), and the superior laryngeal nerve (SLN). The laryngeal
mucosae are mainly supplied by the SLN, and the pharyngeal mucosa is
supplied by a complicated plexus of nerves, namely the pharyngeal
plexus. The pharyngeal plexus is mainly formed by the X-ph and the
pharyngeal branch of the GPN (GPN-ph). The organization of the plexus
varies with the species of animals and even across individuals within a
species (5, 8).
Many previous studies that have examined the role of the
pharyngolaryngeal region in swallowing have employed electrical
stimulation of the peripheral nerves that innervate this area (2,
3, 11, 12, 14). Electrical stimulation of the SLN can readily elicit reflex swallowing (2, 11, 22-24); however, it
is much more difficult for stimulation of the GPN to evoke swallowing than it is for stimulation of the SLN to do so (3, 22).
This ineffectiveness of the GPN to initiate swallowing is somewhat paradoxical if the GPN innervates the pharynx, because mechanical stimulation of the pharyngeal mucosa is very effective in initiating swallowing (3, 15, 21). Sinclair (22) studied
the role of the pharyngeal plexus in the initiation of swallowing in
the cat and concluded that the GPN is the primary afferent for
swallowing from the pharynx. However, it appears that his results and
discussion are somewhat complicated. We can, for instance, find in his
results that electrical stimulation of a cephalic X-ph (designated
branch 22a by Sinclair) elicits reflex swallowing very
easily; the effectiveness of the nerve in the initiation of swallowing
is equivalent to that of the SLN. Sinclair's paper finds, however,
that, although electrical stimulation of the GPN elicits reflex
swallowing, the GPN is much less effective than branch 22a
in this regard. It, therefore, seems that his conclusion is not reasonable.
To resolve the paradox in the initiation of swallowing and to make
clear the contradiction in the results of Sinclair (22), the present study was designed to 1) precisely examine the
reflexogenic areas of swallowing in the pharyngolaryngeal region;
2) identify the afferent pharyngeal branch that contributes
to swallowing from the pharynx; and 3) investigate the
electrophysiological properties of the GPN-ph in initiating swallowing.
Rats were used as the experimental animals in this study because the
pharyngeal nerve plexus of the rat appears to be relatively simple.
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METHODS |
Experiments were carried out with the use of 25 male Wistar rats
weighing 200-400 g. The animals were anesthetized with urethane (1.0 g/kg ip) and placed in the supine position. Body temperature was
maintained at 37°C with a heating pad. A longitudinal midline incision was made in the ventral surface of the neck. The trachea of
the animal was cannulated to maintain respiration. Two unipolar electromyographic (EMG) electrodes made of Enamel-Nichrome wire were
placed in the mylohyoid muscle to record the EMG activity. Swallowing
was identified by the EMG activity of the mylohyoid muscle and by
visual observation of the laryngeal movement. After these procedures
were performed, the following two experiments were carried out.
Identification of afferent nerves innervating the reflexogenic
areas for swallowing in the pharynx and larynx.
To identify the afferent nerve for reflex swallowing in the
pharyngolaryngeal areas, eight rats were used. The SLNs were
bilaterally exposed by blunt dissection of the sternothyroid muscle.
The GPNs were bilaterally exposed by removal of the digastric muscles
and posterior horn of the hyoid bones. These nerves were then dissected free from the surrounding tissue bilaterally. Because the GPN is
composed of the lingual branch of the GPN (GPN-li) and the GPN-ph,
these branches were carefully bilaterally isolated. The pharynx was
surgically opened from the ventral aspect of the pharynx. The mucosae
of the larynx, epiglottis, and pharynx were exposed to determine the
reflexogenic areas for swallowing. The pharyngeal and laryngeal mucosae
were stimulated by application of light pressure (1.0, 5.0, 10, 15, and
20 mN) with a von Frey hair, 0.2 mm in diameter, to elicit reflex
swallowing. The areas from which swallowing was elicited by a probing
stimulation with the von Frey hair were illustrated in a diagram of the
pharyngolaryngeal region. After the reflexogenic areas of swallowing
were examined in the intact GPN-li, GPN-ph, X-ph, and SLN, the afferent
nerves to elicit swallowing from these areas were investigated by
selective sectioning of the GPN-li, GPN-ph, X-ph, and SLN bilaterally.
Electrophysiological properties of the GPN-ph for reflex
swallowing.
Experiments were performed on 17 rats. After the SLN, GPN-li, and
GPN-ph were bilaterally severed, bipolar platinum wire electrodes were
unilaterally fitted onto the central cut end of the GPN-li, GPN-ph, or
SLN to stimulate these nerves. The nerves were stimulated by repetitive
electrical stimulation with a rectangular pulse (intensity:
0.1-3.0 V, frequency: 1.0-100 Hz, duration: 1.0 ms). The
latency for the first swallow was defined as the time required to evoke
the first swallow from the onset of electrical stimulation. The time
interval between the first and third swallows was also measured. The
time interval divided by 2 was considered to be the mean value of the
time intervals (mean time interval of swallows). The latencies for the
first swallow and the mean time intervals between swallows for the
GPN-li and GPN-ph were compared with those of the SLN.
In 5 of 17 rats, electrical stimulation of the GPN-li was applied, in
addition to the stimulation of the SLN, so that the contributions of
afferent signals from the GPN-li for swallowing induced by the SLN
could be examined.
Statistical analysis was performed by using Student's
t-test. Differences with P < 0.05 were
considered statistically significant.
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RESULTS |
Reflexogenic areas of swallowing in the pharyngolaryngeal region.
Reflex swallowing was elicited by mechanical stimulation of the
pharyngeal and laryngeal mucosae with a von Frey hair. Reflexogenic areas for swallowing from the pharyngolaryngeal region are shown in
Fig. 1. The most effective areas were the
palatopharyngeal arch, the posterior edge of the soft palate (an area
extending from the palatopharyngeal arch), the edge of the pharyngeal
surface of the epiglottis, and the aryepiglottic fold. Mechanical
stimulation of these areas elicited swallowing readily with a stimulus
of 1.0 mN. In the moderately reflexogenic areas (the pharyngeal surface of the epiglottis and the posterior pharyngeal wall), the swallowing was initiated with a stimulus of 10 mN. It was difficult to evoke any
reflex swallowing from the other areas. However, when regions adjoining
reflexogenic areas were stimulated with 10, 15, or 20 mN, swallows were
occasionally observed, but body movements were sometimes also observed.
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Fig. 1.
Receptive areas of the pharyngolarynx from which reflex swallowing
was induced by mechanical stimulation with a von Frey hair. The most
reflexogenic areas were the palatopharyngeal arch, the edge of the soft
palate in the pharyngeal region, and the edge of the epiglottis and
aryepiglottic fold. The moderately reflexogenic areas included the
pharyngeal surface of the epiglottis and the posterior pharyngeal wall.
Reflex swallowing was initiated with stimuli of 1.0 mN in the most
reflexogenic area and with stimuli of 10 mN in the moderately
reflexogenic areas.
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Figure 2 illustrates the schematic
description of the GPN-li, GPN-ph, and SLN. The GPN-ph originates from
the trunk of the GPN and anastomoses with X-ph, forming the pharyngeal
plexus. When the SLN was bilaterally sectioned, reflex swallowing from the epiglottis and the aryepiglottic fold was abolished. After the
GPN-ph was sectioned, mechanical stimulation failed to elicit reflex
swallowing from the posterior pharyngeal wall, the palatopharyngeal arch, or the posterior edge of the soft palate (an area extending from the palatopharyngeal arch). Bilateral sectioning of the
GPN-li, as well as of the X-ph, had no effect on the elicitation of
swallowing from the pharyngolaryngeal region. These results indicate
that the GPN-ph is a primary afferent for reflex swallowing from the pharynx.
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Fig. 2.
Diagram
showing the pharyngeal branches of the glossopharyngeal nerve (IX) and
vagus nerve (X) in the rat. GPN-ph, pharyngeal branch of the
glossopharyngeal nerve; GPN-li, lingual branch of the glossopharyngeal
nerve; SLN, superior laryngeal nerve; X-ph, pharyngeal branch of the
vagus nerve. Arrows indicate the sites to which electrical stimulation
was applied.
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Electrophysiological properties of the GPN-ph, SLN, and GPN-li for
reflex swallowing.
Adequate stimulation of the GPN-ph and of the SLN to elicit swallowing
was found to be 0.3-0.7 V and 30-70 Hz at 1.0-ms duration. When both nerves were stimulated with adequate stimulation, reflex swallowing was elicited with short latency (less than ~0.5 s) and was
characterized by successive swallowing. When both nerves were
electrically stimulated (0.3-0.7 V, 1.0 ms) at low (1.0-20 Hz) or high (80-100 Hz) frequency, the stimulation sometimes
failed to initiate successive swallows. Electrical stimulation of both nerves at low voltages (0.1-0.2 V) seldom initiated swallowing. Electrical stimulation of the GPN-ph or the SLN at high voltages (0.8-3.0 V) resulted in reflex swallowing, but swallowing was sometimes accompanied by body movements.
A typical example of reflex swallowing elicited by electrical
stimulation (0.5 V, 30 Hz, 1.0 ms) of the GPN-ph is shown in Fig.
3A. Several swallows were
evoked successively by the stimulation. To compare the effectiveness of
GPN-ph stimulation with that of SLN stimulation, electrical stimulation
of the SLN was also examined. Stimulation of the GPN-ph elicited
sequential swallows similar to those elicited by SLN stimulation (Fig.
3B). The latency of the first swallow for the GPN-ph was
0.38 s, whereas it was 0.22 s for the SLN. The mean time
intervals of swallows induced by the GPN-ph and SLN were 0.81 and
0.73 s, respectively (Fig. 3, A and B).
Electrical stimulation of the GPN-li failed to evoke reflex swallowing
but occasionally induced body movements without swallowing (Fig.
3C). When electrical stimulation was applied simultaneously
to both the SLN and GPN-li, the latency of the first reflex swallow was
delayed, and the time intervals between swallows were prolonged
compared with the reflex swallowing elicited by the SLN alone (Fig. 3,
B and D).
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Fig. 3.
Typical examples of electromyographic (EMG) recordings from the
mylohyoid muscle during swallowing. A and B:
successive swallows elicited by electrical stimulation (0.5 V, 30 Hz,
1.0 ms) of the GPN-ph and SLN, respectively. C: EMG activity
during stimulation of the GPN-li (0.5 V, 20 Hz, 1.0 ms). D:
swallows elicited by simultaneous electrical stimulation of the SLN
(0.5 V, 30 Hz, 1.0 ms) and GPN-li (0.5 V, 40 Hz, 1.0 ms). Note that no
swallows were observed in C and that swallowing induced by
electrical stimulation of the SLN was delayed and prolonged by
electrical stimulation of the GPN-li in D.
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The latency of the first swallow and the mean time interval of swallows
changed with the frequency of electrical stimulation. The relationships
between the stimulus frequency and both the latency of the first
swallow and the mean time interval of swallows were obtained by
administering electrical stimulation at 0.5 V, 10-70 Hz, and 1.0 ms. The relationships shown in Figs. 4
and 5 were obtained from 17 animals.
The latency of the first swallow and the mean time interval between
swallows for the GPN-ph and SLN decreased as the frequency of
electrical stimulation increased, until the frequency reached ~30 Hz.
Once the frequency exceeded 30 Hz, no changes in reflex swallowing were
observed. There were no significant differences in effectiveness in the
elicitation of swallowing between the GPN-ph and the SLN across the
range of frequencies from 10 to 70 Hz.
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Fig. 4.
Relationships between the frequency of electrical
stimulation and the latency of the first swallow for the GPN-ph and
SLN. Electrical stimulation was applied at 0.5 V, 1.0 ms. Each value
represents the mean ± SE (n = 17). No differences
were observed between the GPN-ph and SLN in the latency of the first
swallow across frequencies ranging from 10 to 70 Hz (t-test,
P > 0.05).
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Fig. 5.
Relationships between the frequency of electrical
stimulation and the mean time interval between swallows for the GPN-ph
and SLN. Electrical stimulation was applied at 0.5 V, 1.0 ms. Each
value represents the mean ± SE (n = 17). No
differences were observed between the GPN-ph and SLN in the mean time
interval between swallows across frequencies ranging from 10 to 70 Hz
(t-test, P > 0.05).
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When electrical stimulation of the GPN-li (0.5 V, 10-100 Hz, and
1.0 ms) was applied in addition to the stimulation (0.5 V, 30 Hz, and
1.0 ms) of the SLN, reflex swallowing was delayed or inhibited, as
shown in Fig. 3D. Figure 6
shows the inhibitory effect of the GPN-li on swallowing. When the
GPN-li was stimulated simultaneously with the SLN, the latency of the
first swallow was 0.57 ± 0.08 s (mean ± SE) at 30 Hz
and 1.25 ± 0.11 s at 40 Hz (n = 5), whereas
the latency of the first swallow for the SLN alone was 0.38 ± 0.05 s (n = 17). When the GPN-li was stimulated at
frequencies >50 Hz, in addition to stimulation of the SLN, body
movements were induced without swallowing.
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Fig. 6.
Inhibitory effect of electrical stimulation of the GPN-li
on the elicitation of reflex swallowing by electrical stimulation of
the SLN. The SLN was stimulated at 30 Hz, 0.5 V, 1.0 ms. The GPN-li was
stimulated at 30 or 40 Hz, 0.5 V, 1.0 ms. Each value represents the
mean ± SE (t-test, P < 0.05).
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DISCUSSION |
The present findings, based on mechanical stimulation of the
pharyngeal region, showed that the most sensitive areas for reflex swallowing were the palatopharyngeal arch, the posterior pharyngeal wall, and the posterior edge of the soft palate (an area extending from
the palatopharyngeal arch). It has been shown that the posterior pillars, posterior pharyngeal wall, and nasopharynx were the most reflexogenic areas for swallowing in cats (21). Pommerenke
(17) reported that the tonsillar pillars and the posterior
pharyngeal wall were effective in eliciting reflex swallowing in
humans. The present findings conformed with those for cats and humans.
Denervation experiments in the present study clearly show that the
pharyngeal reflexogenic areas are innervated by the GPN-ph and that the
laryngeal reflexogenic areas, such as the pharyngeal surface of the
epiglottis and the aryepiglottic fold, are innervated by the SLN,
whereas the GPN-li (the main trunk of the GPN) and the X-ph are not
associated with the elicitation of swallowing. Sinclair
(21) reported that sectioning of the GPN in cats abolished the swallowing reflex in the pharynx in only five out of nine animals.
Further sectioning of the X-ph abolished reflex swallowing completely
in the rest of the animals. In contrast, the present results indicate
that the GPN-ph alone is the afferent for reflex swallowing from the
pharynx in rats. The afferent of the X-ph is not associated with the
elicitation of swallowing from the pharynx in our denervation
experiments. This finding is supported by the previous studies.
Anatomic studies demonstrated that afferent fibers are not found in the
X-ph in cat and rats (6, 16). Physiological study reported
that electrical stimulation of the X-ph does not elicit any
cardiovascular responses in rats (7). Therefore, it may be
considered that the X-ph consists of efferent fibers.
The present study revealed that electrical stimulation of the GPN-ph
was very effective in inducing swallowing. The effectiveness of the
GPN-ph in evoking swallowing was almost the same as that of the SLN
(Figs. 4 and 5). In Sinclair's result (22), he reported that electrical stimulation of branch 22a (a cephalic X-ph)
was effective in initiating swallowing. It seems that this is
because the X-ph has an anastomosis with the GPN-ph, and, therefore,
branch 22a consists of both the GPN-ph and X-ph. Previous
studies have reported that stimulation of the GPN can elicit
swallowing, but the effect is less constant, and swallowing is less
readily evoked than in stimulation of the SLN (3, 22).
This finding has been seen as somewhat paradoxical. Sinclair
(22) stated that electrical stimulation of the GPN (i.e.,
the main trunk of the GPN, designated GPN19 by Sinclair) elicited
reflex swallowing with great difficulty compared with stimulation of
the SLN in the cat. The latency of the first swallow and the time
required to initiate three successive swallows were much longer when
the GPN was stimulated than when the SLN was stimulated. However, in
the present study, we showed that the GPN-ph was as effective as the
SLN in eliciting swallowing, whereas electrical stimulation of the
GPN-li (the main trunk to the tongue) did not evoke swallowing (Fig.
3C).
Several reports have claimed that stimulation of the GPN inhibits the
elicitation of swallowing by stimulation of the SLN (1,
25). We also demonstrated that electrical stimulation of the
GPN-li inhibited reflex swallowing elicited by stimulation of the SLN
(Figs. 3D and 6). These findings suggest that the GPN-li contains the inhibitory fibers for the initiation of swallowing. According to anatomic studies (14), the main trunk of the
GPN in cats consists of lingual branches and small pharyngeal branches. It can be assumed, therefore, that, when electrical stimulation was
applied to the main trunk of the GPN, the stimulatory effect of the
small pharyngeal branch may have been inhibited by the lingual branch.
These findings probably explain why electrical stimulation of the GPN
elicits reflex swallowing with more difficulty than does stimulation of
the SLN.
In conclusion, the present study revealed that the most reflexogenic
areas for swallowing in the pharyngeal region in rats were innervated
by the GPN-ph and that the effectiveness of the GPN-ph in evoking
swallowing by electrical stimulation is comparable to that of the SLN.
These results indicate that the GPN-ph, but not the GPN-li, plays a
major role in the initiation of reflex swallowing from the pharynx.
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ACKNOWLEDGEMENTS |
This study was supported by Research for the Future Program (no.
JSPS-RETF97L00906) from the Japan Society for the Promotion of Science.
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FOOTNOTES |
Address for reprint requests and other correspondence: J. Kitagawa, Dept. of Oral Physiology, Niigata Univ. Faculty of Dentistry, 2-5274 Gakkocho-dori, Niigata 951-8514, Japan (E-mail:
kitagawa{at}dent.niigata-u.ac.jp).
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
10.1152/ajpregu.00556.2001
Received 13 September 2001; accepted in final form 12 December 2001.
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REFERENCES |
1.
Comline, RS,
and
Titchen DA.
Reflex contraction of oesophageal groove in young ruminants.
J Physiol (Lond)
115:
210-226,
1951.
2.
Doty, RW.
Influence of stimulus pattern on reflex deglutition.
Am J Physiol
166:
142-158,
1951.
3.
Doty, RW.
Neural organization of deglutition.
In: Handbook of Physiology. Alimentary Canal. Motility. Bethesda, MD: Am. Physiol. Soc, 1968, sect. 6, vol. IV, chapt. 92, p. 1861-1902.
4.
Doty, RW,
and
Bosma JF.
An electromyographic analysis of reflex deglution.
J Neurophysiol
19:
44-60,
1956.
5.
Dubner, R,
Sessle BJ,
and
Story AT.
The Neural Basis of Oral and Facial Function. New York: Plenum, 1978.
6.
Hamilton, RB,
and
Norgren R.
Central projections of gustatory nerves in the rat.
J Comp Neurol
222:
560-577,
1684.
7.
Hanamori, T,
and
Ishiko N.
Cardiovascular responses to gustatory and mechanical stimulation of the nasopharynx in rats.
Brain Res
619:
214-222,
1993.
8.
Hogg, ID,
and
Bryant JW.
The development of sensory innervation in the mouth and pharynx of the albino Norway rat.
J Comp Neurol
136:
33-56,
1969.
9.
Jia, YX,
Sekizawa K,
Ohrui T,
Nakayama K,
and
Sasaki H.
Dopamine D1 receptor antagonist inhibits swallowing reflex in guinea pigs.
Am J Physiol Regulatory Integrative Comp Physiol
274:
R76-R80,
1998.
10.
Jin, Y,
Sekizawa K,
Fukushima T,
Morikawa M,
Nakazawa H,
and
Sasaki H.
Capsaicin desensitization inhibits swallowing reflex in guinea pigs.
Am J Respir Crit Care Med
149:
261-263,
1994.
11.
Kahn, RH.
Studien über den schluckreflex.
Arch Physiol
27, Suppl:
386-426,
1903.
12.
Miller, AJ.
Characteristics of swallowing reflex induced by peripheral nerve and brain stem stimulation.
Exp Neurol
34:
210-222,
1972.
13.
Miller, AJ.
Deglution.
Physiol Rev
62:
129-184,
1982.
14.
Miller, AJ.
The Neuroscientific Principles of Swallowing and Dysphagia. San Diego, CA: Singular, 1999.
15.
Miller, FR,
and
Sherrington CS.
Some observations on the buccopharyngeal stage of reflex deglutition in the cat.
Q J Exp Physiol
9:
147-186,
1916.
16.
Nomura, S,
and
Mizuno N.
Central distribution of efferent and afferent components of the cervical branches of the vagus nerve.
Anat Embryol (Berl)
166:
1-18,
1683.
17.
Pommerenke, WT.
A study of the sensory areas eliciting the swallowing reflex.
Am J Physiol
84:
36-41,
1928.
18.
Pouderoux, P,
Logemann JA,
and
Kahrilas PJ.
Pharyngeal swallowing elicited by fluid infusion: role of volition and vallecular containment.
Am J Physiol Gastrointest Liver Physiol
270:
G347-G354,
1996.
19.
Shingai, T,
Miyaoka Y,
Ikarashi R,
and
Shimada K.
Swallowing reflex elicited by water and taste solutions in humans.
Am J Physiol Regulatory Integrative Comp Physiol
256:
R822-R826,
1989.
20.
Shingai, T,
and
Shimada K.
Reflex swallowing elicited by water and chemical substances applied in the oral cavity, pharynx and larynx of the rabbit.
Jpn J Physiol
26:
455-469,
1976.
21.
Sinclair, WJ.
Initiation of reflex swallowing from the naso- and oropharynx.
Am J Physiol
218:
956-960,
1970.
22.
Sinclair, WJ.
Role of the pharyngeal plexus in initiation of swallowing.
Am J Physiol
221:
1260-1263,
1971.
23.
Storey, AT.
Laryngeal initiation of swallowing.
Exp Neurol
20:
359-365,
1968.
24.
Storey, AT.
A functional analysis of sensory units innervating epiglottis and larynx.
Exp Neurol
20:
366-383,
1968.
25.
Teitelbaum, HA,
and
Ries FA.
A study of the comparative physiology of the glossopharygeal nerve respiratory reflex in rabbit, cat and dog.
Am J Physiol
112:
684-689,
1935.
26.
Travers, JB,
and
Norgren R.
Electromyographic analysis of the ingestion and rejection of sapid stimuli in the rat.
Behav Neurosci
100:
544-555,
1986.
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ABSTRACT
INTRODUCTION
