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Swallowing induces sequential activation of esophageal longitudinal smooth muscle.

We examined the mechanical activity of the longitudinal and circular muscles of the esophagus at three different levels (9, 5, and 1 cm above the lower esophageal sphincter) during peristalsis induced by swallows or vagal stimulation in anesthetized opossums with miniature strain gauges applied in the axis of muscle fibers. The onset of longitudinal muscle contraction occurred in an aboral sequence with swallows but simultaneously with vagal stimulation. The speed of longitudinal muscle activation with swallows was 7.6 +/- 1.7 cm/s. Circular muscle contraction occurred in an aboral sequence with vagal stimulation and swallowing with speeds of 4.1 +/- 0.8 and 2.3 +/- 0.1 cm/s, respectively. Longitudinal muscle contracted before the circular muscle at all sites. The duration of longitudinal muscle contraction increased aborally (P less than 0.05) with swallowing or vagal stimulation. These studies show that 1) during swallowing, esophageal longitudinal and circular smooth muscle contract in a sequential fashion, 2) the longitudinal muscle sequential contraction is due to central mechanisms, whereas circular muscle sequential contraction may be due to both central and peripheral mechanisms, and 3) peripheral neuromuscular mechanisms produce regional differences in the duration of longitudinal muscle contraction.

Animals↗

Volitional augmentation of upper esophageal sphincter opening during swallowing.

Studies were done on eight normal subjects with synchronized videofluoroscopy and manometry to facilitate a biomechanical analysis of the extent and mechanism of voluntary augmentation of upper esophageal sphincter (UES) opening during swallowing. Movements of the hyoid and larynx, dimensions of sphincter opening, and intraluminal pressure events were determined at 1/30-s intervals during swallows of 1 and 10 ml of liquid barium. Swallows of each volume were obtained both before and after subjects were taught a maneuver designed to augment UES opening, the Mendelsohn maneuver (voluntary prolongation of laryngeal excursion at the midpoint of the swallow). At either volume, use of the maneuver increased the duration of the anterior-superior excursion of the larynx and hyoid and consequently delayed sphincter closure by maintaining traction on the anterior sphincter wall. The onset of the pharyngeal contraction (the event normally culminating in sphincter closure) was not affected by the maneuver. We conclude that swallow-related hyoid motion, laryngeal motion, and UES opening are subject to volitional augmentation, supporting the notion that biofeedback techniques can be used to modify impaired swallowing.

Adult↗

Swallowing and upper esophageal sphincter contraction with transcranial magnetic-induced electrical stimulation.

This study in three dogs explores the effect of magnetically induced electrical stimulation of the brain to induce swallowing and produce contraction of the upper esophageal sphincter (UES). Single stimuli were delivered at intervals from 15 s to 3 min. Studies were performed with and without perfusion of fluid into the pharynx and upper esophagus. Results showed that magnetic stimulation produced a twitch contraction of the UES when stimulus intensity was above a threshold that varied between 14 and 20% of the stimulator output. Increasing stimulus intensity progressively increased twitch amplitude. Magnetic stimulation also induced swallowing, above a stimulus threshold similar to that for induction of the UES twitch contraction. Fluid perfusion augmented the ability of the magnetic stimulus to induce swallowing. We concluded that a magnetically induced single electrical stimulus of the cerebral cortex produces UES contraction and induces swallowing. The effect on swallowing is facilitated by sensory stimulation of the pharynx. This technique holds the potential for further study of 1) motor and sensory neural mechanisms involved in the control of swallowing and 2) the assessment and management of oropharyngeal dysphagia in humans.

Animals↗

Physiology of oropharyngeal swallow in the cat: a videofluoroscopic and electromyographic study.

The majority of animal studies of deglutition have examined electrically stimulated swallows in sedated animals. This present investigation examined oropharyngeal and cervical esophageal swallow physiology in three awake normal domestic cats using concurrent electromyography (EMG) and videofluorography (VFG). Hooked wire electrodes were surgically implanted into six oropharyngeal muscles in each cat. During collection of VFG and EMG data, each cat ate barium-impregnated cat food while the fluorography tube focused on a lateral view of the oral cavity, pharynx, and cervical esophagus. A number of significant differences in the physiology of swallowing were found between the cat and human adult. The oral stage of swallow is much longer in the cat with bolus accumulation in the valleculae. Duration and components of the pharyngeal stage of swallow are much faster, and the pharyngeal stage occurs earlier in relation to bolus passage through the cricopharyngeus. In addition, the cat exhibits a marked superior constrictor bulge at the onset of the pharyngeal contractile wave and summation of the peristaltic waves in the esophagus, whereas the human adult does not. Feline swallow physiology is more similar to that of the human infant than that of human adults.

Animals↗

Effects of upper airway stimulation on swallowing, gasping, and autoresuscitation in hypoxic mice.

Severe hypoxia produces a state of neural depression known as hypoxic coma in which reflex activity is believed to be absent but from which spontaneous recovery ("autoresuscitation") still can occur. We evaluated the swallowing reflex during hypoxic coma by employing mechanical and chemosensory stimuli. BALB/c mice were given 97% N2-3% CO2 to breathe. At onset of coma, a 0.05-ml bolus of saline or water was infused into the pharynx. Unlike mechanical stimulation (sham infusion), fluid infusion usually was followed by rapid swallowing, more so with water than with saline. This model allowed examination of interactions among swallowing, hypoxic gasping, airway fluid removal, and autoresuscitation. Compared with sham infusion, saline and water reduced gasping rate equally. Saline, however, prolonged the process of autoresuscitation more than did water, an effect possibly related to an observed increased retention of saline in the airway. Occasionally, mice failed to swallow after infusions, in which case airway obstruction during gasping and autoresuscitation failure was repeatedly observed. These studies suggest that the swallowing component of the laryngeal chemoreflex is present during hypoxic coma and that swallowing facilitates autoresuscitation when upper airway fluid is present.

Animals↗

Electromyographic activity from human laryngeal, pharyngeal, and submental muscles during swallowing.

The durations and temporal relationships of electromyographic activity from the submental complex, superior pharyngeal constrictor, cricopharyngeus, thyroarytenoid, and interarytenoid muscles were examined during swallowing of saliva and of 5- and 10-ml water boluses. Bipolar, hooked-wire electrodes were inserted into all muscles except for the submental complex, which was studied with bipolar surface electrodes. Eight healthy, normal, subjects produced five swallows of each of three bolus volumes for a total of 120 swallows. The total duration of electromyographic activity during the pharyngeal stage of the swallow did not alter with bolus condition; however, specific muscles did show a volume-dependent change in electromyograph duration and time of firing. Submental muscle activity was longest for saliva swallows. The interarytenoid muscle showed a significant difference in duration between the saliva and 10-ml water bolus. Finally, the interval between the onset of laryngeal muscle activity (thyroarytenoid, interarytenoid) and of pharyngeal muscle firing patterns (superior pharyngeal constrictor onset, cricopharyngeus offset) decreased as bolus volume increased. The pattern of muscle activity associated with the swallow showed a high level of intrasubject agreement; the presence of somewhat different patterns among subjects indicated a degree of population variance.

Adult↗

Lung volume effects on pharyngeal swallowing physiology.

The experiment was a prospective, repeated-measures design intended to determine how the variation of lung volume affects specific measures of swallowing physiology. Swallows were recorded in 28 healthy subjects, who ranged in age from 21 to 40 yr (mean age of 29 yr), by using simultaneous videofluoroscopy, bipolar intramuscular electromyography, and respiratory inductance plethysmography. Each subject swallowed three standardized pudding-like consistency boluses at three randomized lung volumes: total lung capacity, functional residual capacity, and residual volume. The results showed that pharyngeal activity duration of deglutition for swallows produced at residual volume was significantly longer than those occurring at total lung capacity or at functional residual capacity. No significant differences were found for bolus transit time or intramuscular electromyography of the superior constrictor. The results of this experiment lend support to the hypothesis that the respiratory system may have a regulatory function related to swallowing and that positive subglottic air pressure may be important for swallowing integrity. Eventually, new treatment paradigms for oropharyngeal dysphagia that are based on respiratory physiology may be developed.

Adult↗

Contributions from rostral medullary nuclei to coordination of swallowing and breathing in awake goats.

The purpose of this study was to determine whether neurons in the facial (FN), gigantocellularis reticularis (RGN), and vestibular (VN) nuclei contribute to the regulation of breathing, swallowing, and the coordination of these two functions. Microtubules were chronically implanted bilaterally in goats. Two weeks later during wakefulness, 100-nl unilateral injections were made of mock cerebral spinal fluid or an excitatory amino acid receptor agonist or antagonists. When the agonist, N-methyl-D-aspartic acid, was injected into any nuclei, breathing and swallowing increased transiently (15-30%; P < 0.05), whereas only injections of the antagonist 2,3-dihydroxy-6-nitro-7-sulfamoylbenzo-(f)quinoxaline into VN increased swallowing (20%; P < 0.05). The phase of breathing in which the swallows occurred was not altered by any injections. However, more importantly, injections of the agonist and the antagonists significantly altered (P < 0.05) by 5-50% the respiratory phase-dependent timing and tidal volume effect of swallows on breathing relative to mock cerebral spinal fluid injections. In addition, these effects were not uniform for all three nuclei. We conclude that the FN, RGN, and VN are part of a neural circuit in the rostral medulla that regulates and/or modulates breathing, swallowing, and their coordination in the awake state.

2-Amino-5-phosphonovalerate↗

Swallow-evoked action potentials in vagal preganglionic efferents.

Swallow-evoked potentials in the preganglionic vagal fibers were studied using the single-fiber recording technique in anesthetized opossums. Swallows were evoked by tactile pharyngeal stimulation or electrical stimulation of the cut central end of the superior laryngeal nerve (SLN). Swallowing activity was recorded by the mylohyoid electromyogram and esophageal motility. Sixty-six fibers were studied in which swallowing evoked action potentials. The latencies (from the onset of mylohyoid activity) of evoked responses in different fibers varied from 100 ms to 5 s. The discharge rate of the evoked response was 3-8 action potentials per burst. Each burst lasted 1.1 +/- 0.02 (SE)s. The latencies of evoked spike bursts showed a bimodal distribution. In 34 fibers the latencies were less than 1 s, and in 32 fibers the latencies ranged between 1 and 5 s; these are the short- and long-latency fibers, respectively. Short-latency fibers could easily be distinguished from long-latency fibers based on the influence of SLN-stimulus frequency. Short-latency discharges had low thresholds of activation and were sensitive to changes in the frequency of SLN stimulation, since their latencies decreased and their discharge rate increased with increasing SLN-stimulus frequency. On the other hand, the latencies and discharge rates of long-latency discharges were not modified with changing SLN stimulus frequencies. The conduction velocities of 6 short- and 9 long-latency fibers were 5.64 +/- 0.12 and 5.78 +/- 0.12 (SE) m/s, respectively (P greater than 0.05). The relationship between the latencies of swallow-evoked discharges in the short- and long-latency fibers and the esophageal smooth muscle responses suggested that the short-latency discharges may correlate with the latency of initial inhibition, and the long-latency fibers may correlate with latencies of peristaltic contractions. Based on these temporal relationships, we speculate that vagal efferent fibers showing swallow-evoked, short-latency discharges make contact with intramural inhibitory neurons. They may mediate deglutitive inhibition in the body of the esophagus, relaxation of the lower esophageal sphincter, and receptive relaxation of the fundus of the stomach. The fibers showing late discharges make contact with intramural excitatory neurons and participate in their sequential activation. This dual pathway of activation may be responsible for physiological esophageal peristalsis.

Animals↗

Modification in activity of medullary respiratory-related neurons for vocalization and swallowing.

1. The medullary ventral respiratory group (VRG) in and near the nucleus ambiguus contains neurons related to respiration. Also found here are neurons related to vocalization and swallowing as well as motoneurons of laryngeal, pharyngeal, palatal, and esophageal muscles. Previous reports in anesthetized animals have characterized discharge properties of neurons as they relate to a single behavior, e.g., respiration. Relatively few studies have documented discharge properties during more than one behavior, e.g., respiration and swallowing. Neurons were recorded extracellularly from awake Macaca nemestrina monkeys engaged in a vocalization task. The present paper describes how respiratory-related neurons (RRNs) modify their discharge during vocalization and swallowing. 2. The temporal relation between vocalization, subglottal pressure (SP), and diaphragm electromyogram (EMG) was established from recordings in anesthetized monkeys. Vocalization was elicited by electrical stimulation of the midbrain periaqueductal gray (PAG). Vocalization is preceded by deep inspiration and a brief pause in diaphragm EMG and begins with a rapid increase in positive SP. 3. Extracellularly recorded neural potential from the VRG in three awake monkeys were related to respiration by correlating their discharge with EMGs from the posterior cricoarytenoid or intercostal muscles during quiet respiration. Neurons were classified as inspiratory (INSP; N = 27), phase spanning (PS; N = 20), or expiratory (N = 6) on this basis. 4. A fourth category of cells was defined as a subgroup of INSP cells on the basis of their discharge during vocalization. This group, inspiratory-pause (INSP-PS; N = 10), paused for approximately 100 ms just before vocalization and resumed their activity during vocalization. 5. Of 63 fully analyzed RRNs, 40 (63%) also modulated their activity with vocalization and 3 (5%) with swallowing. Thirteen (21%) RRNs modulated with vocalization, respiration, and swallowing. Seven (11%) cells were modulated only with respiration. 6. Most cells demonstrated a shorter period of activity and a higher discharge rate associated with vocalization in comparison with quiet respiration. Six (30%) of the PS cells demonstrated an augmenting discharge pattern before vocalization, which was different from the other PS cells and different from their pattern during quiet respiration. Thirteen RRNs showed a pause in activity during vocal fold closure associated with swallowing, whereas three cells gave a burst at this time. 7. The higher discharge rate and shorter burst duration preceding vocalization, compared with quiet respiration, may be related to the greater positive SP necessary to support vocalization.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Identification of the cerebral loci processing human swallowing with H2(15)O PET activation.

Lesional and electrophysiological data implicate a role for the cerebral cortex in the initiation and modulation of human swallowing, and yet its functional neuroanatomy remains undefined. We therefore conducted a functional study of the cerebral loci processing human volitional swallowing with 15O-labeled water positron emission tomography (PET) activation imaging. Regional cerebral activation was investigated in 8 healthy right handed male volunteers with a randomized 12-scan paradigm of rest and water swallows (5 ml/bolus, continuous infusion) at increasing frequencies of 0.1, 0.2, and 0.3 Hz, which were visually cued and monitored with submental electromyogram (EMG). Group and individual linear covariate analyses were performed with SPM96. In five of eight subjects, the cortical motor representation of pharynx was subsequently mapped with transcranial magnetic stimulation (TMS) in a posthoc manner to substantiate findings of hemispheric differences in sensorimotor cortex activation seen with PET. During swallowing, group PET analysis identified increased regional cerebral blood flow (rCBF) (P < 0.001) within bilateral caudolateral sensorimotor cortex [Brodmann's area (BA) 3, 4, and 6], right anterior insula (BA 16), right orbitofrontal and temporopolar cortex (BA 11 and 38), left mesial premotor cortex (BA 6 and 24), left temporopolar cortex and amygdala (BA 38 and 34), left superiomedial cerebellum, and dorsal brain stem. Decreased rCBF (P < 0.001) was also observed within bilateral posterior parietal cortex (BA 7), right anterior occipital cortex (BA 19), left superior frontal cortex (BA 8), right prefrontal cortex (BA 9), and bilateral superiomedial temporal cortex (BA 41 and 42). Individual PET analysis revealed asymmetric representation within sensorimotor cortex in six of eight subjects, four lateralizing to right hemisphere and two to left hemisphere. TMS mapping in the five subjects identified condordant interhemisphere asymmetries in the motor representation for pharynx, consistent with the PET findings. We conclude that volitional swallowing recruits multiple cerebral regions, in particular sensorimotor cortex, insula, temporopolar cortex, cerebellum, and brain stem, the sensorimotor cortex displaying strong degrees of interhemispheric asymmetry, further substantiated with TMS. Such findings may help explain the variable nature of swallowing disorders after stroke and other focal lesions to the cerebral cortex.

Adult↗

Normal swallowing physiology as viewed by videofluoroscopy and videoendoscopy.

This study examines normal oropharyngeal swallow physiology in 8 young adult males with concurrent videofluoroscopy and videoendoscopy. Twelve swallows were examined for each subject, 3 swallows each of 1 and 5 ml of thin liquid at each of two endoscopic positions: (1) the tip of the endoscope just at or below the tip of the uvula (high position), and (2) the tip of the endoscope just below the tip of the epiglottis (low position). Results indicate that if the clinician is interested in laryngeal events occurring before and after swallow, videoendoscopy with the endoscope in the low position is the procedure of choice. To evaluate pharyngeal anatomy and/or the presence of food in the pharynx before or after swallow, either endoscopy with the endoscope in the high position or videofluoroscopy can be used. However, if the clinician is interested in pharyngeal physiology during swallow, videofluoroscopy is a better diagnostic procedure.

Adult↗

Ovine fetal swallowing and behavioral state responses to sublingual water.

Ovine fetal swallowing primarily occurs in bouts of activity associated with low voltage electrocorticogram activity and breathing movements. Despite similar rates of electromyographic swallowing activity, there are significant differences in the net esophageal fluid flow among fetuses. To determine if variations in the volume of fluids accessible to the fetus (amniotic fluid, lung fluid, salivary secretions) affect fetal swallowing, we studied the effects of sublingual distilled water infusions on ovine fetal swallowing rates and esophageal flow. Seven pregnant ewes at 127 +/- 2 days gestation were chronically instrumented with maternal and fetal vascular catheters, fetal electrocortical, electro-ocular and electromyograph electrodes, an esophageal flow probe and a sublingual infusion catheter. Following a 2-hour control period, consecutive sublingual infusions of room temperature distilled water (10 and 20 ml/kg/h) were administered for 2 h each. In response to sublingual infusions, fetal plasma sodium (142.5 +/- 0.5 to 140.8 +/- 0.8 mEq/l), chloride concentrations (109.2 +/- 0.4 to 107.7 +/- 0.7 mEq/l) and osmolality (302 +/- 2 to 298 +/- 2 mOsm/kg) decreased significantly. Swallowing activity and esophageal flow did not change significantly from basal values (47 +/- 9 swallows/h, 19.2 +/- 4.2 ml/h) during the sublingual infusions. However, fetal low-voltage electrocortical activity increased significantly during both infusion periods (42 +/- 3 to 56 +/- 6%). Sublingual distilled water infusion decreases fetal plasma osmolality and alters fetal behavioral state without affecting swallowing frequency or esophageal flow.

Administration, Sublingual↗

Control of ventilation during continuous swallowing.

The upper airway performs three distinct functions that must be coordinated to allow maximal operation of each individual system. We tested the ventilatory response to progressive hypercapnia in seven normal adults during continuous swallowing. Swallowing was induced by oral infusion of water while the subject breathed through the nose. Infusion of 40 ml/min resulted in repetitive swallows (rate: 8.1 +/- 4.1 swallows/min, mean +/- SD), but this did not cause a single incidence of coughing or aspiration. Swallows interrupted inspiration and expiration and resulted in compensatory changes in tidal volume and breathing frequency. Continuous drinking did not significantly change the slope of the ventilatory response to hypercapnia. The test was repeated in three subjects swallowing water infused at 60, 80, and 100 ml/min. The slope of the response was also not significantly different from control in these tests. We conclude that continuous swallowing does not override ventilatory control mechanisms in human adults.

Carbon Dioxide↗

Physiologic effects of open and closed tracheostomy tubes on the pharyngeal swallow.

Studies linking aspiration and dysphagia to an open tracheostomy tube exemplify the possibility that the larynx may have an influence on oropharyngeal swallow function. Experiments addressing the effects of tracheostomy tube occlusion during the swallow have looked at the presence and severity of aspiration, but few have included measurements that capture the changes in swallowing physiology. Also, hypotheses for the importance of near-normal subglottic air pressure during the swallow have not been offered to date. As such, the aim of this study was to compare the depth of laryngeal penetration, bolus speed, and duration of pharyngeal muscle contraction during the swallow in individuals with tracheostomy tubes while their tubes were open and closed. The results of this series of experiments indicate that within the same tracheostomized patient, pharyngeal swallowing physiology is measurably different in the absence of subglottic air pressure (open tube) as compared to the closed tube condition.

Aged↗

Swallowing-related perihypoglossal neurons projecting to hypoglossal motoneurons in the cat.

Although previous studies have examined the functional role of the neurons in the area ventrolateral to the hypoglossal nucleus (perihypoglossal neurons) in the trigemino-hypoglossal reflex, no convincing evidence for the direct connection from the perihypoglossal neurons to the hypoglossal motoneurons has yet been provided. In addition, the role of the perihypoglossal neurons in swallowing has not been studied. The purpose of this study was to investigate (1) the input-output relationship of the perihypoglossal neurons and (2) whether the afferent feedback was essential for their swallowing-related activity in chloralose-anesthetized cats. Before and after the cats were paralyzed, single-unit activities were recorded extracellularly from 30 perihypoglossal neurons during swallowing elicited by electrical stimulation of the superior laryngeal nerve. These perihypoglossal neurons responded with spike potentials after short latencies to stimulation of the inferior alveolar and hypoglossal nerves. The neurons also responded with spike potentials to single shocks applied to the superior laryngeal nerve, but were activated transiently at the initial phase of repetitive stimulation of the nerve and kept silent until the occurrence of swallowing before and after the animal was paralyzed. They showed burst activities in coincidence with swallowing. Averaging of intracellular potentials of a hypoglossal motoneuron by simultaneously recorded extracellular spikes of a perihypoglossal neuron revealed monosynaptic inhibitory post-synaptic potentials. We conclude that, in the region ventrolateral to the hypoglossal nucleus, there are neurons which relay trigeminal, hypoglossal, and vagal afferents. Furthermore, some of these perihypoglossal neurons are inhibitory hypoglossal premotor neurons that are involved in the central programming of swallowing.

Afferent Pathways↗

Assessments of fetal swallowed volume: tracer disappearance versus esophageal flow.

OBJECTIVE: We sought to compare fetal swallowed volume determinations simultaneously by two techniques--amniotic fluid (AF) tracer disappearance and esophageal flow probe measurements. METHODS: Six ovine fetuses (129 +/- 1 days) were chronically prepared with a thoracic esophageal flow probe and vascular and two AF catheters. 125I-labeled albumin was injected into the AF cavity, and samples were withdrawn at timed intervals for 8 hours. The AF volume was calculated by time-0 extrapolation of the semilog of 125I disappearance. Tracer-determined swallowed volume was calculated as the product of AF volume and the slope of isotope disappearance. Flow probe measurement of swallowed volume was determined by computer integration of calibrated flow probe velocity recordings. RESULTS: The AF volume averaged 805 +/- 168 mL. The isotope disappearance rate from the AF was 2.8 +/- 0.4%/hour. Average tracer-determined swallowed volume (547 +/- 113 mL/day) was greater than flow probe volume (366 +/- 81 mL/day), although these values were not significantly different. However, when corrected for estimated swallowed lung fluid, tracer-determined volume was significantly greater than flow probe volume (P < .05). CONCLUSION: Ovine fetal swallowed volume determinations by AF tracer techniques are greater than those determined by esophageal flow probe measurements.

Amniotic Fluid↗

Impedance pharyngography to assess swallowing function.

We evaluated impedance pharyngography (IPG), a new method to assess swallowing function based on changes in the electrical impedance of the neck during swallowing. The electrical impedance of the neck, recorded by the 4-electrode method, changed with the equivalent cross-sectional area of the route of the electric current due to reflex activities of related organs during swallowing. IPG waveforms accurately recorded the swallowing process, therefore. We recommend IPG for assessing swallowing function because we expect IPG to provide the following advantages over conventional diagnostic techniques: it is a quantitative method that allows for the objective assessment of swallowing function; it is a simple procedure that is convenient for the patient and could be used for screening; it is inexpensive and non-invasive, so could be performed repeatedly in situations such as rehabilitation; and it uses highly portable equipment suitable for community use.

Adult↗