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1 Department of Oral Physiology, Okayama University Dental School, Okayama 700-8525; and 2 Okayama Prefectural University Junior College, Soja 719-1197, Japan
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The response of gastric motility to the administration of water and saline in the larynx and epiglottis was investigated in urethan-chloralose anesthetized rats. Administration of water inhibited motility of the distal stomach, but 0.15 M NaCl did not induce the inhibitory response. Bilateral sectioning of the superior laryngeal nerve (SLN) abolished the inhibitory response induced by water. Bilateral cervical vagotomies abolished the inhibitory responses, although spinal transection did not affect the inhibitory response. These inhibitory responses have been observed in immobilized animals. The degree of inhibition by water and hypotonic saline was negatively correlated with the sodium concentration. In contrast, the degree of inhibition to hypertonic saline was positively correlated with the sodium concentration. The proximal stomach also showed a reduction in intragastric pressure in response to the administration of water. These findings suggest that water-responsive afferent neurons in the SLN suppress gastric motility via the vagal efferent nerve.
stomach; superior laryngeal nerve; vagal nerve; relaxation
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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REDUCTION IN GASTRIC TONE is mediated, in part, by the extrinsic nervous system. Mechanical stimulation of antrum stretch receptors reduces intragastric pressure (1). Osmolarity, caloric density, and macronutrient content inhibit gastric motility or slow gastric emptying, suggesting the presence of intestinal chemoreceptors (4, 15, 21). Thus ingesta either mechanically or chemically stimulate abdominal receptors to cause a reduction in gastric tone. In addition, gastric relaxation can occur before food reaches the stomach and facilitates the reservoir function of the stomach. Cannon and Lieb (9) demonstrated relaxation of the canine stomach during swallowing. Mechanical stimulation of the pharynx and distension of the esophagus had been assumed to induce such relaxation (2). Thus swallowed food itself stimulates the upper alimentary tract, causing relaxation of the stomach.
The afferent neurons in the superior laryngeal nerve (SLN), which bifurcates from the vagal nerve, are responsible for protective reflexes such as apnea (40) and reflex swallowing (39). The SLN, which innervates taste buds distributed on the laryngeal surface of the epiglottis and on the larynx, responds to mechanical and chemical stimulation of the larynx and epiglottis (40). Taste buds distributed on the larynx are anatomically similar to those found throughout the oral cavity (44). However, because of their location, it is unlikely that they are involved in conscious taste sensation. Individual fibers of the SLN are broadly chemosensitive as are other gustatory nerves (8, 38). The most obvious difference between the sensitivities of chemosensitive fibers of the SLN and those in other gustatory nerves is in the response to water (8, 20, 38). Several studies have suggested that afferent neurons in the SLN responding to water are involved in important functions, such as diuresis, prandial drinking, and cardiovascular responses (18, 29, 37). These nerves convey sensory information to the caudal portion of nucleus of the solitary tract (NTS) near the dorsal motor nucleus of the vagus (DMV), where vagal preganglionic neuron cell bodies are located (16, 19, 41). Because the vagal preganglionic neurons in the dorsomedial medulla are considered to regulate various gastric functions (12, 22), the SLN might affect gastric motility and/or relaxation via the vagus nerve.
The present study was undertaken to clarify the role of the superior laryngeal afferent signals elicited by water and saline on gastric motility. The effect of laryngeal stimulation by water and saline on gastric contractility was investigated. Their neural mechanisms were also considered.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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General methods. Animal care was in accordance with the guidelines of the Physiological Society of Japan. Male Sprague-Dawley rats (8-10 wk) were used. Each animal was fasted for 1 day to empty the stomach before the experiment was started. Each animal was anesthetized with an intraperitoneal injection of urethan-chloralose (urethan, 0.8 g/kg; chloralose, 65 mg/kg body wt). Subsequent anesthesia was administered as required through an unocclusive catheter constructed from the tip of an injection needle (23 gauge) and Silastic tubing (OD: 1.0 mm, ID: 0.5 mm) inserted into the right jugular vein. Each animal had a tracheal cannula made from polyethylene tubing (OD: 2.07 mm). The esophagus was ligated to prevent the test solutions from entering the stomach. Animals were placed in the supine position during the course of the experiments.
After an abdominal incision was made, an intragastric balloon, created from thin latex rubber and plastic tubing (OD: 1.7 mm), was introduced into the stomach from the greater curvature just proximal to the limiting ridge toward the antrum (Fig. 1). The balloon was secured by purse sutures around the gastric wall using 4-0 silk thread. At the end of each experiment, the abdomen was reopened and the position of the balloon was confirmed. Balloons were always positioned in the body of the stomach. Another tubing (OD: 2.0 mm) was also introduced into the fundus to drain the gastric juices and was ligated with the gastric wall around the tubing. The gastric balloon was inflated with warm water at 37°C to a volume of 3.0 ml/kg body wt. Before each experiment, it was confirmed that this volume of water did not induce pressure in the balloon outside the body. This volume was comparable to that used in a previous study (23). After inflation of the gastric balloon, animals were left for at least 20 min until the gastric contraction was stabilized. The distal end of this tubing was connected with a strain-gauge pressure meter (NEC-Sanei, 6M82) to measure intragastric pressure.
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Electrical stimulation. In seven animals, inhibition of gastric motility induced by the electrical stimulation of the SLN was observed. The sternohyoid and omohyoid muscles were retracted. The SLNs were isolated from the surrounding tissue and bilaterally sectioned. The central cut end of the SLN was stimulated using a repeat electric pulse (20 Hz, 0.3 ms in duration, 0.3 mA in intensity) for 20 s using platinum bipolar electrodes.
SLN sections. To determine the ascending pathway, both SLNs were sectioned in six animals. Before the experiments, both SLNs were isolated from the surrounding tissue. After evaluation of the inhibition of contractile activity by the administration of water, sectioning of both SLNs was performed. Sectioning of the SLNs always induced a transient decrease in intragastric pressure that returned to the presectioning level after a few minutes. After stabilization of gastric contractility, water was again administered.
Vagotomy and splanchnicotomy. To determine the descending pathway, vagotomies were performed in five animals. Both vagi were carefully separated from the left and right carotid arteries. After evaluation of the inhibition of the contractile activity induced by the administration of water, sectioning of both vagi was performed. Both vagi were sectioned at the cervical level below where the SLN entered the vagal trunk, allowing their afferent signals into the central nervous system. More than 10 min after the sectioning, the response of gastric contractility to administration of water was measured again. Specific verification of successful nerve sectioning was not performed, because these nerves can be observed with a binocular microscope. Both vagotomies induced a gradual increase in intragastric tone and slowed the respiratory phase.
In addition, transection of the spinal cord was performed in seven animals. Before each experiment, the spinal cord was exposed by removing the spinal process and arches of T3 and T4. After evaluation of the inhibition of the contractile activity by the administration of water, the exposed spinal cord was sectioned between T3 and T4 using a microspatula. Sixty minutes after the transection, the response of gastric contractility to the administration of water was measured again. The portion of sectioning of each animal was confirmed visually at the end of each experiment.Concentration-response function. To further examine the characteristics of the effects of different concentrations of saline on gastric motility, stimuli of water and eight concentrations of saline solutions were given in 15 animals. Different methods for the administration of the test solutions were used for these experiments. Both the chorda tympani and glossopharyngeal nerves innervate taste buds (13, 17). Therefore, each animal underwent bilateral sectioning of the chorda tympani and glossopharyngeal nerves before the surgery for recording intragastric pressure to prevent the test solutions activating these nerves. Both tympanic membranes were punctured, and the mallei were removed. Then, the chorda tympani nerves were sectioned. The glossopharyngeal nerves were exposed by partial removal of the hyoid process and carefully dissected from the surrounding tissue. Then, both glossopharyngeal nerves were sectioned between the external and internal carotid arteries. Polyethylene tubing (OD: 2.3 mm, ID: 1.5 mm) attached to a 15-gauge injection needle, was introduced into the trachea rostrally and fixed by 3-0 silk suture. Test solutions (1.0 ml) were water or 0.01, 0.03, 0.1, 0.15, 0.3, 0.5, or 1.0 M NaCl and were manually administered at room temperature. Injections of solutions were completed in 20 s. The responses to water were tested in all animals used for this series of experiments. After administration of water, each animal received more than two different concentrations of saline solutions. Saline solutions were delivered in ascending order of sodium concentration. Two minutes after each stimulus, 0.15 M NaCl (1.0 ml) was injected twice to wash out the test solutions. Motility returned to the preinjection level a few minutes after washing. The interval of stimulus was at least 20 min. Injected solutions were allowed to flow into the oral cavity. Other studies (8, 38) used a flow and suction system to apply and remove the stimuli to record afferent discharge from the SLN after sectioning both SLNs to avoid reflex swallowing. This method is adequate to remove the stimulant. However, because both SLNs had to be intact in the present research, reflex swallowing induced by the test solutions disrupted removal of the solutions in our preliminary experiments. Therefore, we did not use this flow and suction system.
Artificial ventilation and recordings from the proximal stomach. In this series of experiments, balloons were intubated in the proximal and the distal stomach in six animals. For the intubation of the two balloons in the stomach, large animals (450-500 g) were used. After intubation of the gastric balloon into the distal stomach, similar tubing with an attached balloon was introduced into the fundus from the minor curvature (Fig. 1). The gastric balloon situated in the proximal stomach was inflated with 0.5 ml water (37°C). The gastric balloon situated in the distal stomach was inflated with 0.8 ml water (37°C). A relatively small inflation in the distal stomach was achieved to prevent the two balloons influencing each other. Therefore, the contraction waves obtained were smaller than those in other experiments. The other procedure was similar to when intragastric pressure of the distal stomach was measured alone.
Six animals were neuromuscularly blocked using gallamine triethiodide (10 mg/kg iv, Sigma) and were ventilated with O2-enriched room air and positive end-expiratory pressure using a positive pressure ventilator (Shinano, SN-480-7) to exclude the influence of swallowing and respiration. The end-tidal CO2 pressure of expired gas was continuously measured with a fast-response CO2 analyzer (Cwe, Capstar-100) and was maintained within a range of 30-40 mmHg. Arterial blood pressure was measured through the polyethylene catheter (PE-50, Intramedic) inserted into the left carotid artery and was carefully separated from the vagi. During neuromuscular blockade, the depth of anesthesia was assessed by monitoring the stability of the arterial blood pressure, heart rate, and the cardiovascular responses to pinching the paws.Data analysis. The contractile response was quantified by measuring the area under contractions (kPa × min) using the Flextrace program (Tree Star) on a personal computer. The area was measured at 1-min intervals, starting at the beginning of the injection of the test solution. The area before injection was also measured as a control. The mean values of the area 2 min before administration of the solution and 2 min after were used for comparison between pre- and posttreatment (motility area). For normalizing the data, the ratios of the area between 2 min before injection and 2 min after injection were also used for analyses (motility ratio). All numerical values are represented as means ± SE. Significant differences among the mean motility areas were evaluated using the paired t-test (P < 0.05 for significance). Significant differences between each mean motility ratio and 1.0 was also evaluated using the paired t-test (P < 0.05 for significance).
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Response of gastric motility to water and 0.15 M NaCl.
The administration of 0.15 M NaCl did not induce any change in
contractile activity or intragastric pressure. In contrast, the
administration of water markedly decreased gastric contractility and
the base level of the contraction (Fig.
2A). An inhibition of phasic
contractions was always observed. However, the decreases in the basal
level of the contraction curve shown in Fig. 2A were not
always observed. Inhibition of motility (area under contraction) by
water continued until 5 min after initiation of the injection (Fig.
2B). Significant differences (t = 3.74, P = 0.0033, n = 12 at 0-1 min;
t = 4.24, P = 0.0014, n = 12 at 1-2 min; t = 3.43, P = 0.0056, n = 12 at 2-3 min; t = 2.30, P = 0.0417, n = 12 at 3-4
min; t = 4.09, P = 0.0018, n = 12 at 4-5 min) were observed compared with the
preinjection motility. The difference between the motility after the
administration of water and that of 0.15 M NaCl was significant at 1 min (t = 2.51, P = 0.0199, n = 12) and 2 min (t = 3.59, P = 0.0016, n = 12) after initiation of
the injection. Because motility was markedly inhibited during the first
2 min immediately after the stimulation by water (Fig. 2B), the ratios of the area between 2 min before injection and 2 min after
injection (motility ratio) are presented (Fig. 2C). The mean
motility ratio induced by water (0.62 ± 0.05, n = 12) clearly shows significant inhibition (t = 8.07, P < 0.0001, n = 12), but that by 0.15 M NaCl (1.05 ± 0.07, n = 12) was not significant (t = 0.75, NS, n = 12). These findings
suggested that the inhibition of motility was induced by the
administration of water but not by other mechanical or thermal stimuli.
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Effects of electrical stimulation of the SLN on gastric motility.
Effects of electrical stimulation of the central cut end of each SLN
were investigated. Electrical stimulation markedly inhibited contractility (Fig. 3). Electrical
stimulation caused a relatively rapid decrease in gastric pressure,
which gradually returned to prestimulation levels after cessation of
the stimulation. The mean motility ratio when the left SLN was
stimulated (0.64 ± 0.05, n = 7; t = 7.26, P = 0.0003) and when the right SLN was
stimulated (0.68 ± 0.04, n = 7; t = 8.69, P = 0.0001) was significantly reduced. No
differences were noted between the inhibitory responses induced by
stimulation of the left SLN and those of the right SLN.
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Effects of sectioning the SLN on the inhibitory response of gastric
motility.
To determine the afferent pathway, gastric motility responses to the
administration of water after bilateral sectioning of the SLN were
investigated. No inhibition of motility induced by the administration
of water in animals was observed after sectioning of both SLNs. In
intact animals, the mean motility area for 2 min after the
administration of water (2.60 ± 0.21 kPa × min, n = 6) was significantly smaller (t = 3.30, P = 0.0216, n = 6) than that
before administration (5.36 ± 0.94 kPa × min,
n = 6). After sectioning the SLN, however, no
significant difference was observed (t = 1.40, P = 0.9570, n = 6) between the mean
motility area before the administration of water (4.68 ± 0.96 kPa × min, n = 6) and that after the
administration (4.35 ± 0.96 kPa × min, n = 6). The mean motility ratio observed before sectioning the SLNs was
0.54 ± 0.07 (n = 6) and was ~1.0
(0.93 ± 0.06, n = 6) after sectioning both SLNs
(Fig. 4). A significant
difference in the mean motility ratio was observed before sectioning
the SLNs (t = 6.78, P = 0.0010, n = 6); however, this was not observed after sectioning
the SLNs (t = 1.18, P = 0.2924, n = 6).
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Effects of cervical vagotomy and spinal transection on the
inhibition of gastric motility.
To determine the descending pathway on the inhibition of gastric
motility, experiments were performed on vagotomized or spinal sectioned
animals (Fig. 5). Inhibitory response of
motility shown after administration of water was not observed after
sectioning both vagi at the cervical level. In intact animals, the mean
motility area for 2 min after administration of water (1.54 ± 0.15 kPa × min, n = 5) was significantly smaller
(t = 6.64, P = 0.0012, n = 5) than that before administration (2.52 ± 0.22 kPa × min, n = 5). After bilateral cervical
vagotomy, however, no significant difference was observed
(t = 2.27, P = 0.7250, n = 5) between the mean motility area before
administration of water (1.96 ± 0.23 kPa × min,
n = 5) and that after administration (1.86 ± 0.25 kPa × min, n = 5). The mean motility ratio
observed before sectioning the vagi (0.62 ± 0.04, n = 5) became ~1.0 (0.94 ± 0.03, n = 5) after sectioning of the vagi. A significant
difference in the mean motility ratio was observed before sectioning
the vagi (t = 8.98, P = 0.0420, n = 5); however, this was not observed after sectioning
(t = 2.42, P = 0.7270, n = 5).
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Concentration-response function of the inhibition.
To further examine the characteristics of the effect on gastric
motility, water and different concentrations of saline were administered to the animals that underwent the bilateral sectioning of
both chorda tympani and glossopharyngeal nerves (Fig.
6). The degree of inhibition to water and
hypotonic saline was negatively correlated with the increase in sodium
concentration. In contrast, the degree of inhibition to hypertonic
saline was positively correlated with the increase in sodium
concentration. Differences were significant in the mean motility ratio
when water (t = 8.10, P < 0.0001, n = 15), 0.01 M NaCl (t = 3.20, P = 0.0109, n = 10), 0.03 M NaCl (t = 2.73, P = 0.0232, n = 10), 0.5 M NaCl (t = 2.78, P = 0.0388, n = 6), or 1.0 M NaCl
(t = 14.04, P = 0.0001, n = 9) was administered.
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Inhibitory responses observed in immobilized animals.
The inhibition of gastric motility was observed in immobilized and
artificially ventilated animals. Before artificial respiration, animals
showed a marked inhibition of gastric motility induced by the
administration of water. After administration of gallamine triethiodide, the magnitude of spontaneous phasic contractions was
lowered. As shown in Fig. 7, in voluntary
respiring animals, the mean motility area for 2 min after
administration of water (0.75 ± 0.35 kPa × min,
n = 6) was significantly smaller (t = 3.59, P = 0.0158, n = 6) than that
before administration (1.25 ± 0.47 kPa × min,
n = 6). After the administration of gallamine, the
amplitude of the contraction wave was lowered. The mean motility area
for 2 min after administration of water (0.54 ± 0.28 kPa × min, n = 6) was significantly smaller
(t = 2.59, P = 0.0489, n = 6) than that before administration (0.75 ± 0.35 kPa × min, n = 6). The mean motility ratio
both before (0.51 ± 0.0910, t = 5.35, P = 0.0031, n = 6) and after gallamine
administration (0.71 ± 0.0610; t = 4.80, P = 0.0049, n = 6) showed significant inhibition of gastric motility.
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Response of the proximal stomach.
All observations described above were obtained from the distal stomach.
To clarify the response of the proximal stomach to the administration
of water into the larynx, the change in intragastric pressure in the
proximal stomach in addition to that in the distal stomach was
measured. Figure 8 shows simultaneous
recordings of both the proximal and the distal stomach. The proximal
stomach did not show phasic contraction, but the baseline fell,
indicating a decrease in intragastric pressure after administration of
water but not on administration of 0.15 M NaCl. Similar inhibition of intragastric pressure in the proximal stomach was observed in three
other animals.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The present study showed that the administration of water into the larynx inhibited gastric motility. Phasic contractions in the distal stomach were suppressed, and relaxation of the proximal stomach was induced by the administration of water. Bilateral sectioning of the SLNs abolished the inhibitory response induced by water, as did bilateral sectioning of the cervical vagal nerves. These observations indicate the presence of a vago-vagal reflex arc to the stomach.
Stimulation was induced by the use of a 0.1-ml solution delivered toward the laryngeal surface of the epiglottis in the present study. The targets of the stimuli were the epiglottis and the larynx. A part of the delivered solution may have spread to the pharynx. In the stimulus condition, the inhibitory responses observed after administration of water were eliminated by sectioning both SLNs. Therefore, test solutions were administered, in the present study, to the area innervated by the SLN. The findings obtained from bolus injection of water into the oral cavity of animals that had received bilateral sectioning of the chorda tympani and glossopharyngeal nerves also indicated that the SLNs have a major role in the inhibition of the stomach induced by the administration of water.
It was shown that NaCl solution was effective in increasing the firing
frequency of SLN fibers at concentrations below isotonic saline. The
firing frequency increased with decreasing NaCl concentration (34, 35). Similar findings were seen in the
response of gastric motility in the present study. The degree of
inhibition of gastric motility increased with decreasing sodium
concentrations of the test solution below the isotonic level. In the
present study, significant inhibitions of gastric motility were also
observed after the administration of 0.5 and 1.0 M NaCl. The degree of inhibition increased with increasing concentrations of NaCl in the
hypertonic solution. Smith and Hanamori (38) reported that hamster SLN fibers responded to relatively high concentrations of NaCl
as well as to hypotonic saline. The response of gastric motility shown
in the present study presumably reflects the response characteristics
of primary afferent neurons. Water response is not regarded as a
specific response to water per se. Response to water was attributed to
the sensitivity of the receptor membrane to the outward flow of
Cl
in rabbits and dogs (6, 34).
In mice, the results of responses of SLN fibers to either electrolytes
or nonelectrolytes suggest that water response is induced by the change
in osmolality of the solutions (36). The response
mechanism appears to be different between animal species. In addition,
several studies have demonstrated that SLN fibers in a number of
species respond to epiglottal stimulation with water and other chemical
substances (6, 8, 34,
38). Water-sensitive fibers in the SLN also respond to the
other chemicals. In the present study, although we did not test the
effects of chemicals other than NaCl, chemicals such as HCl or
NH4Cl should induce similar inhibition of gastric motility.
Gastric contractility is regulated by the vagal preganglionic nerve and the splanchnic nerve (27, 32). Excitation of vagal motor fibers may cause either a facilitation or an inhibition of motility, suggesting two kinds of motor fibers (26). Splanchnic nerve sectioning had a lesser effect on motility than that of vagotomy (32). In the present study, bilateral vagotomy at the cervical level completely abolished the inhibitory response of the stomach induced by the administration of water, although afferent invasion of the SLN to the central nervous system remained intact. However, spinal transection did not affect the intragastric pressure. Therefore, the inhibitory response found in the present study resulted in the facilitation or suppression of vagal preganglionic fibers. Anatomical studies reveal that the cell bodies of the vagal motor neurons innervating the stomach are predominantly located at the DMV (11, 30), although additional innervations of nucleus ambiguus (NA) neurons have also been observed (24). Their main innervation targets are the upper alimentary tract, including the larynx, pharynx, and esophagus (3). The NA neurons projecting to the stomach predominantly innervate the forestomach (11, 33). The DMV is probably the most important site to induce the inhibitory response shown in the present study.
Administration of water into the larynx induced reflex apnea and swallowing (39, 40). Proprioceptive units were recorded in the caudal branch of the SLN, which enters the inferior pharyngeal constrictor muscle (16). Modification of afferent discharges by expiration and inspiration in the rostral branch of the SLN was demonstrated (16). It is therefore possible that the inhibitory response of the stomach was caused by changes in neural activity associated with muscle contraction by swallowing and/or the disappearance of the respiratory phase. Some NTS neurons that received inputs from the SLN showed the respiratory firing pattern (10). In the present study, the inhibition of intragastric pressure observed by administration of water was also observed in immobilized animals. Therefore, the inhibitory responses shown in the present study were truly induced by the activation of water-responsive afferents in the SLN and not by proprioceptive activation associated with reflex swallowing or apnea.
Gastric inhibitory response is observed during and after the prandial period. Mechanical stimulation of the gastric antrum induced gastric relaxation (1). Satiety agents, such as CCK inhibit gastric motility (14). Osmolarity, caloric density, or macronutrient content has been suggested to reduce intragastric pressure (4, 15, 21). These agents, associated with food intake, would prevent the intragastric pressure from becoming high during and after food ingestion. Cannon and Lieb (9) demonstrated relaxation of the canine stomach during swallowing, which is the so-called "receptive relaxation." Another effective stimulus is esophageal distension (2, 43). Because these reflexes inhibit intragastric pressure before ingested food or liquid reaches the stomach, they are considered anticipatory responses. These relaxation responses, abolished by vagotomy but not by splanchnicotomy, are similar to those observed in the present study. Water-responsive afferents in the SLN should elicit similar reflexes such as receptive relaxation. Because water intake is an important signal of the initiation of eating, the reflex arc found in the present study might have a role in facilitating gastric relaxation to accommodate the intake of food and liquid similar to receptive relaxation.
Taste buds are especially concentrated on the laryngeal surface of the epiglottis (5, 7, 28). Because taste buds in this region appear to be ideally situated for protecting the airway during accidental aspiration of food or fluid, inhibitory responses of the stomach observed in the present study might be initiated only when fluid is going to invade the larynx. However, aryepiglottal folds and the upper esophagus also contain taste buds in addition to the laryngeal surface of the epiglottis (5, 28, 42). The epithelium of the rostral portion of the pharyngeal mucosa is innervated by the superior laryngeal nerve (25). Taste buds situated in the pharynx or esophagus would be stimulated during normal food or fluid intake. Further investigation using microstimulation of restricted regions might provide better understanding of the physiological functions of the reflex observed in the present study.
Perspectives
Receptive relaxation, which was proposed by Cannon and Lieb (9), is one of the reflexes caused by the extrinsic nervous system during swallowing and facilitates the reservoir function of the stomach. It was suggested that this inhibitory response of the stomach is caused by mechanical stimulation of the pharynx and esophagus by ingesta (2). Water fibers in the SLN might be a novel neuronal source for the receptive relaxation, although more precise experiments are demanded to clarify this. To provide an accurate view of the participation of SLN water fibers in the receptive relaxation, the response of the stomach to the liquid stimulation of the restricted area, which is usually stimulated by food and fluid intake, should be confirmed. Furthermore, the study of central neurons might provide a better understanding of the control mechanisms of gastric motility. Recently, the central neural mechanisms of gastric relaxation and inhibition of gastric motility evoked by esophageal distension was clarified electrophysiologically (31). Esophageal afferents appear to provoke inhibition of the stomach by activating a vagal inhibitory pathway and inhibiting a vagal excitatory pathway. Finally, it is preferable to clarify how oral signals combine with the other sensations that induce the inhibition of the stomach in the central nervous system and induced the conformable inhibitions of the stomach that facilitate the reservoir functions of stomach.| |
FOOTNOTES |
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Address for reprint requests and other correspondence: M. Kobashi, Dept. of Oral Physiology, Okayama Univ. Dental School, 2-5-1 Shikata-cho, Okayama 700-8525, Japan (E-mail: mkobashi{at}dent.okayama-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. §1734 solely to indicate this fact.
Received 13 September 1999; accepted in final form 24 March 2000.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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|---|
1.
Abrahamsson, H.
Vagal relaxation of the stomach induced from the gastric antrum.
Acta Physiol Scand
89:
406-414,
1973[ISI][Medline].
2.
Abrahamsson, H,
and
Jansson G.
Elicitation of reflex vagal relaxation of the stomach from pharynx and esophagus in the cat.
Acta Physiol Scand
77:
172-178,
1969[ISI][Medline].
3.
Altschuler, SM,
Bao X,
and
Miselis RR.
Dendritic architecture of nucleus ambiguus motoneurons projecting to upper alimentary tract in the rat.
J Comp Neurol
309:
402-414,
1991[ISI][Medline].
4.
Azpiroz, F,
and
Malagelada J-R.
Physiological variations in canine gastric tone measured by an electronic barostat.
Am J Physiol Gastrointest Liver Physiol
248:
G229-G237,
1985
5.
Belecky, TL,
and
Smith DV.
Postnatal development of palatal and laryngeal taste buds in the hamster.
J Comp Neurol
293:
646-654,
1990[ISI][Medline].
6.
Boggs, DF,
and
Bartlett D, Jr.
Chemical specificity of a laryngeal apneic reflex in puppies.
J Appl Physiol
53:
455-462,
1982
7.
Bradley, RM,
Cheal M,
and
Kim Y.
Quantitative analysis of developing epiglottal taste buds in sheep.
J Anat
130:
25-32,
1980[ISI][Medline].
8.
Bradley, RM,
Stedman HM,
and
Mistretta CM.
Superior laryngeal nerve response patterns to chemical stimulation of sheep epiglottis.
Brain Res
276:
81-93,
1983[ISI][Medline].
9.
Cannon, WB,
and
Lieb CW.
The receptive relaxation of the stomach.
Am J Physiol
29:
267-273,
1911.
10.
Dawid-Milner, MS,
Silva-Carvalho L,
Goldsmith GE,
and
Spyer KM.
Hypothalamic modulation of laryngeal reflexes in the anaesthetized cat: role of the nucleus tractus solitarii.
J Physiol (Lond)
487:
739-749,
1995[ISI].
11.
Ewart, WR,
Jones MV,
and
King BF.
Central origin of vagal nerve fibres innervating the fundus and corpus of the stomach in rat.
J Auton Nerv Syst
25:
219-231,
1988[ISI][Medline].
12.
Feng, H-S,
Lynn RB,
Han J,
and
Brooks FP.
Gastric effects of TRH analogue and bicuculline injected into dorsal motor vagal nucleus in cats.
Am J Physiol Gastrointest Liver Physiol
259:
G321-G326,
1990
13.
Fish, H,
Malone P,
and
Richter C.
The anatomy of the tongue of the domestic Norway rat. I. The skin of the tongue; the various papillae; their number and distribution.
Anat Rec
89:
429-440,
1944.
14.
Flanagan, LM,
Verbalis JG,
and
Stricker EM.
Effects of anorexigenic treatments on gastric motility in rats.
Am J Physiol Regulatory Integrative Comp Physiol
256:
R955-R961,
1989
15.
Forster, ER,
Green T,
Elliot M,
Bremner A,
and
Dockray GJ.
Gastric emptying in rats: role of afferent neurons and cholecystokinin.
Am J Physiol Gastrointest Liver Physiol
258:
G552-G556,
1990
16.
Furusawa, K,
Yasuda K,
Okuda D,
Tanaka M,
and
Yamaoka M.
Central distribution and peripheral functional properties of afferent and efferent components of the superior laryngeal nerve: morphological and electrophysiological studies in the rat.
J Comp Neurol
375:
147-156,
1996[ISI][Medline].
17.
Guth, L.
Effects of glossopharyngeal nerve transection on the circumvallate papilla of the rat.
Anat Rec
128:
715-731,
1957.
18.
Hanamori, T,
and
Ishiko N.
Cardiovascular responses to gustatory and mechanical stimulation of the nasopharynx in rats.
Brain Res
619:
214-222,
1993[ISI][Medline].
19.
Hanamori, T,
and
Smith DV.
Gustatory innervation in the rabbit: central distribution of sensory and motor components of the chorda tympani, glossopharyngeal, and superior laryngeal nerves.
J Comp Neurol
282:
1-14,
1989[ISI][Medline].
20.
Harada, S,
and
Smith DV.
Gustatory sensitivities of the hamster's soft palate.
Chem Senses
17:
37-51,
1992
21.
Hunt, JN,
and
Stubbs DF.
The volume and energy content of meals as determinants of gastric emptying.
J Physiol (Lond)
245:
209-225,
1975
22.
Laughton, WB,
and
Powley TL.
Localization of efferent function in the dorsal motor nucleus of the vagus.
Am J Physiol Regulatory Integrative Comp Physiol
252:
R13-R25,
1987
23.
Lefebvre, RA,
Hasrat J,
and
Gobert A.
Influence of NG-nitro-L-arginine methyl ester on vagally induced gastric relaxation in the anaesthetized rat.
Br J Pharmacol
1992:
313-320,
1992.
24.
Leslie, DG,
Gwyn DG,
and
Hopkins DA.
The central distribution of the cervical vagus nerve and gastric afferent and efferent projections in the rat.
Brain Res Bull
8:
37-43,
1982[ISI][Medline].
25.
Maeyama, T,
Miyazaki J,
Tsuda K,
and
Shin T.
Distribution and origin of the intraepithelial nerve fibres in the feline pharyngeal mucosa.
Acta Otolaryngol (Stockh)
539:
87-90,
1998.
26.
Martinson, J,
and
Muren A.
Excitatory and inhibitory effects of vagus stimulation on gastric motility in the cat.
Acta Physiol Scand
57:
309-316,
1963[ISI].
27.
Meyer, EA.
The physiology of gastric storage and emptying.
In: Physiology of the Gastrointestinal Tract (3rd ed.), edited by Johnson LR.. NY: Raven, 1994, p. 929-976.
28.
Miller, IJJ,
and
Smith DV.
Quantitative taste bud distribution in the hamster.
Physiol Behav
32:
275-285,
1984[Medline].
29.
Miyaoka, Y,
Sakaguchi T,
Yamazaki M,
and
Shingai T.
Changes in water intake following pharyngolaryngeal deafferentation in the rat.
Physiol Behav
40:
369-371,
1987[Medline].
30.
Okumura, T,
and
Namiki M.
Vagal motor neurons innervating the stomach are site-specifically organized in the dorsal motor nucleus of the vagus nerve in rats.
J Auton Nerv Syst
29:
157-162,
1990[ISI][Medline].
31.
Rogers, RC,
Hermann GE,
and
Travagli RA.
Brainstem pathways responsible for esophageal control of gastric motility and tone in the rat.
J Physiol (Lond)
514:
369-383,
1999
32.
Roman, C,
and
Gonella J.
Extrinsic control of digestive tract motility.
In: Physiology of the Gastrointestinal Tract (2nd ed.), edited by Johnson LR.. NY: Raven, 1987, p. 507-553.
33.
Shapiro, RE,
and
Miselis RR.
The central organization of the vagus nerve innervating the stomach of the rat.
J Comp Neurol
238:
473-488,
1985[ISI][Medline].
34.
Shingai, T.
Ionic mechanism of water receptors in the laryngeal mucosa of the rabbit.
Jpn J Physiol
27:
27-42,
1977[ISI][Medline].
35.
Shingai, T.
Water fibers in the superior laryngeal nerve of the rat.
Jpn J Physiol
30:
305-307,
1980[ISI][Medline].
36.
Shingai, T,
and
Beidler LM.
Response characteristics of three taste nerves in mice.
Brain Res
335:
245-249,
1985[ISI][Medline].
37.
Shingai, T,
Miyaoka Y,
and
Shimada K.
Diuresis mediated by the superior laryngeal nerve in rats.
Physiol Behav
44:
431-433,
1988[Medline].
38.
Smith, DV,
and
Hanamori T.
Organization of gustatory sensitivities in hamster superior laryngeal nerve fibers.
J Neurophysiol
65:
1098-1114,
1991
39.
Storey, AT.
Laryngeal initiation of swallowing.
Exp Neurol
20:
359-365,
1968[ISI][Medline].
40.
Storey, AT,
and
Johnson P.
Laryngeal water receptors initiating apnea in the lamb.
Exp Neurol
47:
42-55,
1975[ISI][Medline].
41.
Sweazey, RD,
and
Bradley RM.
Central connections of the lingual-tonsillar branch of the glossopharyngeal nerve and the superior laryngeal nerve in lamb.
J Comp Neurol
245:
471-482,
1986[ISI][Medline].
42.
Travers, SP,
and
Nicklas K.
Taste bud distribution in the rat pharynx and larynx.
Anat Rec
227:
373-379,
1990[Medline].
43.
Wei, JY,
Wang YH,
Go VLW,
and
Tache Y.
Esophageal distension induced gastric relaxation is mediated in part by vagal peripheral reflex mechanism in rats.
J Auton Nerv Syst
63:
12-18,
1997[ISI][Medline].
44.
Zahm, DS,
and
Munger BL.
Fetal development of primate chemosensory corpuscles. I. Synaptic relationships in late gestation.
J Comp Neurol
213:
146-162,
1983[ISI][Medline].
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, Administration of the
test solutions. Dashed line shows the baseline of the intragastric
pressure. B: gastric motility before and after the
administration of the test solutions. Gastric motility is represented
by the area under the contraction wave every minute. * Significant
difference compared with the value just before administration of the
test solution. 
Significant difference compared with the value
obtained by administration of 0.15 M NaCl at the same period.
C: mean motility ratios between the area just before
administration (for 2 min) and that just after administration (for 2 min) are shown. * Significant difference in the value compared with
1.0.
, Mean motility ratios in the spinal
sectioned group; 
