Effects of spontaneous swallows on breathing in awake goats.

The effects of spontaneous swallows on breathing before, during, and after solitary swallows were investigated in 13 awake goats. Inspiratory (TI) and expiratory (TE) time and respiratory output were determined from inspiratory airflow [tidal volume (VT)] and peak diaphragmatic activity (Dia(peak)). The onset time for 1,128 swallows was determined from pharyngeal muscle electrical activity. During inspiration, the later the swallowing onset, the greater increase in TI and VT, whereas there was no significant effect on TE and Dia(peak). Swallows in early expiration increased the preceding TI and reduced TE, whereas later in expiration swallows increased TE. After expiratory swallows, TI and VT were reduced whereas minimal changes in Dia(peak) were observed. Phase response analysis revealed a within-breath, phase-dependent effect of swallowing on breathing, resulting in a resetting of the respiratory oscillator. However, the shift in timing in the breaths after a swallow was not parallel, further demonstrating a respiratory phase-dependent effect on breathing. We conclude that, in the awake state, within- and multiple-breath effects on respiratory timing and output are induced and/or required in the coordination of breathing and swallowing.     

The interaction between breathing and swallowing in healthy individuals

In this article, we aimed at investigating the interaction between breathing and swallowing patterns in normal subjects. Ten healthy volunteers were included in the study. Diaphragm EMG activity was recorded by a needle electrode inserted into the 7th or 8th intercostal space. Swallowing was monitored by submental EMG activity, and laryngeal vertical movement was recorded by using a movement sensor. A single voluntary swallow was initiated during either the inspiration or expiration phases of respiration, and changes in EMG activity were evaluated. When a swallow coincided with either inspiration or expiration, the duration of the respiratory phase was prolonged. Normal subjects were able to voluntarily swallow during inspiration. During the inspiration phase with swallowing, diaphragmatic activity did not ceased and during the expiration phase with swallowing, there was a muscle activity in the diaphragm muscle.     

Suppression of Abdominal Motor Activity during Swallowing in Cats and Humans

Diseases affecting pulmonary mechanics often result in changes to the coordination of swallow and breathing. We hypothesize that during times of increased intrathoracic pressure, swallow suppresses ongoing expiratory drive to ensure bolus transport through the esophagus. To this end, we sought to determine the effects of swallow on abdominal electromyographic (EMG) activity during expiratory threshold loading in anesthetized cats and in awake-healthy adult humans. Expiratory threshold loads were applied to recruit abdominal motor activity during breathing, and swallow was triggered by infusion of water into the mouth. In both anesthetized cats and humans, expiratory cycles which contained swallows had a significant reduction in abdominal EMG activity, and a greater percentage of swallows were produced during inspiration and/or respiratory phase transitions. These results suggest that: a) spinal expiratory motor pathways play an important role in the execution of swallow, and b) a more complex mechanical relationship exists between breathing and swallow than has previously been envisioned.     

Respiration during feeding on solid food: alterations in breathing during mastication, pharyngeal bolus aggregation, and swallowing.

During feeding, solid food is chewed and propelled to the oropharynx, where the bolus gradually aggregates while the larynx remains open and breathing continues. The aggregated bolus in the valleculae is exposed to respiratory airflow, yet aspiration is rare in healthy individuals. The mechanism for preventing aspiration during bolus aggregation is unclear. One possibility is that alterations in the pattern of respiration during feeding could help prevent inhalation of food from the pharynx. We hypothesized that respiration was inhibited during bolus aggregation in the valleculae. Videofluorography was performed on 10 healthy volunteers eating solid foods with barium. Respiration was monitored concurrently with plethysmography and nasal air pressure. The timing of events during mastication, food transport, pharyngeal bolus aggregation, and swallowing were measured in relation to respiration. Respiratory cycle duration decreased during chewing (P < 0.001) but increased with swallowing (P < 0.001). During 66 recordings of vallecular bolus aggregation, there was inspiration in 8%, expiration in 41%, a pause in breathing in 17%, and multiple phases (including inspiration) in 35%. Out of 98 swallows, 47% started in the expiratory phase and 50% started during a pause in breathing, irrespective of bolus aggregation in the valleculae. Plethysmography was better than nasal manometry for determining the end of active expiration during feeding and swallowing with solid food. The hypothesis is rejected in that respiration was not inhibited during bolus aggregation. These findings suggest that airflow through the pharynx does not have a role in preventing aspiration during bolus aggregation in the oropharynx.     

Coordination of breathing, sucking, and swallowing during bottle feedings in human infants

Incoordination of sucking, swallowing, and breathing might lead to the decreased ventilation that accompanies bottle feeding in infants, but the precise temporal relationship between these events has not been established. Therefore, we studied the coordination of sucks, swallows, and breaths in healthy infants (8 full-term and 5 preterm). Respiratory movements and airflow were recorded as were sucks and swallows (intraoral and intrapharyngeal pressure). Sucks did not interrupt breathing or decrease minute ventilation during nonnutritive sucking. Minute ventilation during bottle feedings was inversely related to swallow frequency, with elimination of ventilation as the swallowing frequency approached 1.4/s. Swallows were associated with a 600-ms period of decreased respiratory initiation and with a period of airway closure lasting 530 +/- 9.8 (SE) ms. Occasional periods of prolonged airway closure were observed in all infants during feedings. Respiratory efforts during airway closure (obstructed breaths) were common. The present findings indicate that the decreased ventilation observed during bottle feedings is primarily a consequence of airway closure associated with the act of swallowing, whereas the decreased ventilatory efforts result from respiratory inhibition during swallows.     

Chest wall motion during epidural anesthesia in dogs

To determine the relative contribution of rib cage and abdominal muscles to expiratory muscle activity during quiet breathing, we used lumbar epidural anesthesia in six pentobarbital sodium-anesthetized dogs lying supine to paralyze the abdominal muscles while leaving rib cage muscle motor function substantially intact. A high-speed X-ray scanner (Dynamic Spatial Reconstructor) provided three-dimensional images of the thorax. The contribution of expiratory muscle activity to tidal breathing was assessed by a comparison of chest wall configuration during relaxed apnea with that at end expiration. We found that expiratory muscle activity was responsible for approximately half of the changes in thoracic volume during inspiration. Paralysis of the abdominal muscles had little effect on the pattern of breathing, including the contribution of expiratory muscle activity to tidal breathing, in most dogs. We conclude that, although there is consistent phasic expiratory electrical activity in both the rib cage and the abdominal muscles of pentobarbital-anesthetized dogs lying supine, the muscles of the rib cage are mechanically the most important expiratory muscles during quiet breathing.     

Perturbations in three medullary nuclei enhance fractionated breathing in awake goats.

Our aim was to determine the frequency and characteristics of a fractionated pattern of diaphragm and upper airway muscle activity and airflow during wakefulness and sleep in adult goats. A fractionated breath (FBr) was defined as three or more brief (40-150 ms) interruptions in the diaphragm activity not associated with multiple swallows, eructation, mastication, or movement. During a FBr, the discharge pattern in the diaphragm and upper airway muscles showed complete cycles of inspiration and expiration. Whereas the interval between peak diaphragm activity of the breath preceding the FBr to the first diaphragm peak of the FBr was 15-20% less than the average interval of the preceding five control breaths, the breath-to-breath interval of the five breaths after a FBr did not differ from the control breaths before the FBr event. In normal goats, FBr was evident in only 4 of 18 (22%) awake goats and in only one of these goats during non-rapid eye movement sleep. In 35 goats with implanted microtubules in the medulla, FBr were present in 14 (40%) goats. In these goats with FBr, 78% (11 of 14) had one or more implantations into or near the facial, vestibular, or raphe nuclei. The effect of perturbations in these nuclei is probably nonspecific, because injections into these nuclei with mock cerebrospinal fluid or excitatory amino acid-receptor agonist or antagonist produced both increases and decreases in the frequency of the FBr while not altering their characteristics. Finally, a swallow occurred at the termination or during the first breath after 60% of the FBr. We speculate that the FBr manifest 1) the disruption of a neuronal network, which coordinates breathing and other functions (such as swallowing), utilizing the same anatomic structures, and/or 2) transient changes in synaptic inputs that increase the rate of the normal respiratory rhythm generator or allow an ectopic, anomalous generator to become dominant.     

Time-dependent responses of expiration reflex in cats

We investigated the effectiveness of the "expiration reflex" in 10 anesthetized spontaneously breathing cats. The expiration reflex was produced by mechanical stimulation of the vocal folds and electrical stimulation of the superior laryngeal nerve at different moments in the respiratory cycle and at various levels of respiratory chemical drive. The effectiveness of the expiration reflex was evaluated from sudden changes in expiratory flow immediately following the stimulation. Both mechanical and electrical stimulations given during early inspiration caused little or no expiratory efforts, whereas stimulations given during early expiration or hypocapnic apnea produced a typical expiration reflex. Changes in arterial CO2 and O2 partial pressures influenced neither the relationships between the stimulation and its effect on the expiration reflex nor the strength of the expiration reflex. These results indicate that the timing of stimulation with relation to the phase of the respiratory cycle is critical to its effect on the expiration reflex and that changes in respiratory chemical drive do not modify the expiration reflex characteristics.     

Respiratory neuronal activity during apnea and other breathing patterns induced by laryngeal stimulation

Respiration cycles through three distinct phases (inspiration, postinspiration, and expiration) each having corresponding medullary cells that are excited during one phase and inhibited during the other two. Laryngeal stimulation is known to induce apnea in newborn animals, but the cellular mechanisms underlying this effect are not known. Intracellular recording of ventral respiratory group neurons was accomplished in intact anesthetized, paralyzed, and mechanically ventilated piglets. Apnea was induced by insufflation of the larynx with ammonia-saturated air, smoke, or water. Laryngeal insufflation induced phrenic nerve apnea, stimulation of postinspiratory neurons, and stable membrane potentials in inspiratory and expiratory cells consistent with postinspiratory inhibition. Usually the membrane potential of each neuronal type cycled through an expiratory level before onset of the first recovery breath. Variants of the apnea response, probably reflecting the aspiration reflex or sniffing, sneezing, coughing, and swallowing, were also observed. These latter patterns showed oscillation between inspiration and postinspiration without an apparent intervening stage II expiratory phase. However, stage II expiratory activity always preceded onset of the first ramp inspiration after such a pattern. These findings suggest that activation of postinspiratory mechanisms causes profound alterations in the respiratory pattern and that stage II expiration importantly modulates recovery of ramp inspiratory activity. The mechanism of this latter effect may be inhibition of early inspiratory neurons with consequent postinhibitory rebound.     

Breathing strategy of the adult horse (Equus caballus) at rest

To investigate the mechanism underlying the polyphasic airflow pattern of the equine species, we recorded airflow, tidal volum, rib cage and abdominal motion, and the sequence of activation of the diaphragm, intercostal, and abdominal muscles during quiet breathing in nine adult horses standing at rest. In addition, esophageal, abdominal, and transdiaphragmatic pressures were simultaneously recorded using balloon-tipped catheters. Analysis of tidal flow-volume loops showed that, unlike humans, the horse at rest breathes around, rather than from, the relaxed volume of the respiratory system (Vrx). Analysis of the pattern of electromyographic activities and changes in generated pressures during the breathing cycle indicate that the first part of expiration is passive, as in humans, with deflation toward Vrx, but subsequent abdominal activity is responsible for a second phase of expiration: active deflation to below Vrx. From this end-expiratory volume, passive inflation occurs toward Vrx, followed by a second phase of inspiration: active inflation to above Vrx, brought about by inspiratory muscle contraction. Under these conditions the abdominal muscles appear to share the principal pumping duties with the diaphragm. Adoption of this breathing strategy by the horse may relate to its peculiar thoracoabdominal anatomic arrangement and to its very low passive chest wall compliance. We conclude that there is a passive and active phase to both inspiration and expiration due to the coordinated action of the respiratory pump muscles responsible for the resting adult horse's biphasic inspiratory and expiratory airflow pattern. This unique breathing pattern perhaps represents a strategy of minimizing the high elastic work of breathing in this species, at least at resting breathing frequencies.     

Adaptation of swallowing hyo-laryngeal kinematics is distinct in oral vs. pharyngeal sensory processing

Before a bolus is pushed into the pharynx, oral sensory processing is critical for planning movements of the subsequent pharyngeal swallow, including hyoid bone and laryngeal (hyo-laryngeal) kinematics. However, oral and pharyngeal sensory processing for hyo-laryngeal kinematics is not fully understood. In 11 healthy adults, we examined changes in kinematics with sensory adaptation, sensitivity shifting, with oropharyngeal swallows vs. pharyngeal swallows (no oral processing), and with various bolus volumes and tastes. Only pharyngeal swallows showed sensory adaptation (gradual changes in kinematics with repeated exposure to the same bolus). Conversely, only oropharyngeal swallows distinguished volume differences, whereas pharyngeal swallows did not. No taste effects were observed for either swallow type. The hyo-laryngeal kinematics were very similar between oropharyngeal swallows and pharyngeal swallows with a comparable bolus. Sensitivity shifting (changing sensory threshold for a small bolus when it immediately follows several very large boluses) was not observed in pharyngeal or oropharyngeal swallowing. These findings indicate that once oral sensory processing has set a motor program for a specific kind of bolus (i.e., 5 ml water), hyo-laryngeal movements are already highly standardized and optimized, showing no shifting or adaptation regardless of repeated exposure (sensory adaptation) or previous sensory experiences (sensitivity shifting). Also, the oral cavity is highly specialized for differentiating certain properties of a bolus (volume) that might require a specific motor plan to ensure swallowing safety, whereas the pharyngeal cavity does not make the same distinctions. Pharyngeal sensory processing might not be able to adjust motor plans created by the oral cavity once the swallow has already been triggered.     

Thyroarytenoid muscle activity during loaded and nonloaded breathing in adult humans

Previous fiber-optic studies in humans have demonstrated narrowing of the glottic aperture in expiration during application of expiratory resistive loads. Nine healthy subjects were studied to determine the effect of expiratory resistive loads on the electromyographic activity of the thyroarytenoid (TA) muscle, a vocal cord adductor. Four of the nine subjects also underwent the application of inspiratory resistive loads and voluntary prolongation of either inspiratory (TI) or expiratory (TE) time. TA activity was recorded by intramuscular hooked-wire electrodes. During quiet breathing in all subjects, the TA was phasically active on expiration and often tonically active throughout the respiratory cycle. TA expiratory activity progressively increased with increasing levels of expiratory load. Inspiratory loads resulted in increased TA "inspiratory" activity. Voluntary prolongation of TE to times similar to those reached during loaded breathing induced increases in TA expiratory activity similar to those reached during the loaded state. Voluntary prolongation of TI was associated with an increase in TA inspiratory activity. Similar increases in TI during inspiratory loading or voluntary conditions were associated with comparable increases in TA inspiratory activity in three of the four subjects. In conclusion, increased activation of TA during the application of expiratory resistive loads implies that the reported narrowing of glottic aperture during expiratory loading is an active phenomenon. Changes in activation of the TA with resistive loads appear to be related to changes in respiratory pattern.     

Control of larynx during loaded breathing in normal subjects

We examined laryngeal resistance (Rla) in six normal subjects in control and four kinds of loaded breathing: hypercapnia, chest strapping, added external resistance, and inhaled methacholine. Rla was measured with a low-frequency sound methed (Sekizawa et al., J. Appl. Physiol. 55: 591-597, 1983). In control and the four kinds of loaded breathing, changes in Rla were tightly coupled with ventilation and Rla decreased during inspiration and increased during expiration. Hypercapnia and chest strapping significantly decreased Rla in both inspiration and expiration in all subjects. Added external resistance decreased inspiratory Rla in all subjects, but decreased expiratory Rla in three subjects, did not change it in two subjects, and increased it in one subject. Inhaled methacholine increased Rla in both inspiration and expiration in all subjects. The present study suggests that although laryngeal movement is tightly coupled with ventilation, laryngeal aperture may be determined by the complex competition of dilating and constricting mechanisms associated with the activity of the respiratory center and neural reflexes from the airway.     

The effect of posture on respiratory activity of the abdominal muscles

The purpose of this study was to determine the influence of posture on the expiratory activity of the abdominal muscles. Fifteen young adult men participated in the study. Activities of the external oblique abdominis, internal oblique abdominis, and rectus abdominis muscles were measured electromyographically in various postures. We used a pressure threshold in order to activate the abdominal muscles as these muscles are silent at rest. A spirometer was used to measure the lung volume in various postures. Subjects were placed in the supine, standing, sitting, and sitting-with-elbow-on-the-knee (SEK) positions. Electromyographic activity and mouth pressure were measured during spontaneous breathing and maximal voluntary ventilation under the respiratory load. We observed that the lung volume changed with posture; however, the breathing pattern under respiratory load did not change. During maximal voluntary ventilation, internal oblique abdominis muscle expiratory activity was lower in the SEK position than in any other position, external oblique abdominis muscle inspiratory activity was lower in the supine position than in any other position, and internal oblique abdominis muscle activity was higher in the standing position than in any other position. During spontaneous breathing, external oblique abdominis muscle activity was higher during expiration and inspiration in the SEK position than in any other position. The internal oblique abdominis muscle activity was higher during both inspiration and expiration in the standing position than in any other position. The rectus abdominis muscle activity did not change with changes in posture during both inspiration and expiration. Increase in the external oblique abdominis activity in the SEK position was due to anatomical muscle arrangement that was consistent with the direction of lower rib movement. On the other hand, increase in the internal oblique abdominis activity in the standing position was due to stretching of the abdominal wall by the viscera. We concluded that differences in activity were due to differences in the anatomy of the abdominal muscles and the influence of gravity.     

The breathing pattern after breath-holding: the influence of chest position and the drive to breathe.

The pattern of breathing following the breaking-point of sixty breath-holds has been studied in five healthy adults and compared with the pattern during recovery from CO2-rebreathing. The volume and direction of the first respiratory movement, and the VT, V relation for the first four complete breaths was measured. Only when breath-holds were terminated with an inspiration was the accumulated drive to breathe reflected in an increased volume of the first respiratory movement: terminating expirations simply returned the chest to the resting respiratory level. The volume of the first inspiration was not influenced by the intervention of a terminating expiration, suggesting that expiratory movements do not dissipate the non-chemical component of the drive to breathe. In three of the five subjects the tidal volumes for given levels of ventilation were greater following breath-holding than following rebreathing. This altered pattern of breathing has been interpreted in terms of an insiratory-augmenting reflex.     

Postinspiratory activity of costal and crural diaphragm.

Because the first stage of expiration or "postinspiration" is an active neurorespiratory event, we expect some persistence of diaphragm electromyogram (EMG) after the cessation of inspiratory airflow, as postinspiratory inspiratory activity (PIIA). The costal and crural segments of the mammalian diaphragm have different mechanical and proprioceptive characteristics, so postinspiratory activity of these two portions may be different. In six canines, we implanted chronically EMG electrodes and sonomicrometer transducers and then sampled EMG activity and length of costal and crural diaphragm segments at 4 kHz, 10.2 days after implantation during wakeful, resting breathing. Costal and crural EMG were reviewed on-screen, and duration of PIIA was calculated for each breath. Crural PIIA was present in nearly every breath, with mean duration 16% of expiratory time, compared with costal PIIA with duration -2. 6% of expiratory time (P < 0.002). A linear regression model of crural centroid frequency vs. length, which was computed during the active shortening of inspiration, did not accurately predict crural EMG centroid frequency values at equivalent length during the controlled relaxation of postinspiration. This difference in activation of crural diaphragm in inspiration and postinspiration is consistent with a different pattern of motor unit recruitment during PIIA.     

Effects of augmented respiratory muscle pressure production on locomotor limb venous return during calf contraction exercise.

We determined effects of augmented inspiratory and expiratory intrathoracic pressure or abdominal pressure (Pab) excursions on within-breath changes in steady-state femoral venous blood flow (Qfv) and net Qfv during tightly controlled (total breath time = 4 s, duty cycle = 0.5) accessory muscle/"rib cage" (DeltaPab <2 cmH2O) or diaphragmatic (DeltaPab >5 cmH2O) breathing. Selectively augmenting inspiratory intrathoracic pressure excursion during rib cage breathing augmented inspiratory facilitation of Qfv from the resting limb (69% and 89% of all flow occurred during nonloaded and loaded inspiration, respectively); however, net Qfv in the steady state was not altered because of slight reductions in femoral venous return during the ensuing expiratory phase of the breath. Selectively augmenting inspiratory esophageal pressure excursion during a predominantly diaphragmatic breath at rest did not alter within-breath changes in Qfv relative to nonloaded conditions (net retrograde flow = -9 +/- 12% and -4 +/- 9% during nonloaded and loaded inspiration, respectively), supporting the notion that the inferior vena cava is completely collapsed by relatively small increases in gastric pressure. Addition of inspiratory + expiratory loading to diaphragmatic breathing at rest resulted in reversal of within-breath changes in Qfv, such that >90% of all anterograde Qfv occurred during inspiration. Inspiratory + expiratory loading also reduced steady-state Qfv during mild- and moderate-intensity calf contractions compared with inspiratory loading alone. We conclude that 1) exaggerated inspiratory pressure excursions may augment within-breath changes in femoral venous return but do not increase net Qfv in the steady state and 2) active expiration during diaphragmatic breathing reduces the steady-state hyperemic response to dynamic exercise by mechanically impeding venous return from the locomotor limb, which may contribute to exercise limitation in health and disease.     

Maximum airflow through the nose in humans

Inspiratory and expiratory flow via the nose and via the mouth during maximum-effort vital capacity (VC) maneuvers have been compared in 10 healthy subjects. Under baseline conditions maximum flow via the nose was lower than that via the mouth in the upper 50-60% of the VC on expiration and throughout the VC on inspiration. The mean ratio of maximum inspiratory to maximum expiratory flow at mid-VC was 1.38 during mouth breathing and 0.62 during nasal breathing. Inspiratory flow limitation with no increase in flow through the nose as driving pressure was increased above a critical value (usually between 12 and 30 cmH2O) was found in all six subjects studied. Stenting the alae nasi in seven subjects increased peak flow via the nose from a mean of 3.49 to 4.32 l/s on inspiration and from 4.83 to 5.61 l/s on expiration. Topical application of an alpha-adrenergic agonist in seven subjects increased mean peak nasal flow on inspiration from 3.25 to 3.89 l/s and on expiration from 5.03 to 7.09 l/s. Further increases in peak flow occurred with subsequent alan stenting. With the combination of stenting and topical mucosal vasoconstriction, nasal peak flow on expiration reached 81% and, on inspiration, 79% of corresponding peak flows via the mouth. The results demonstrate that narrowing of the alar vestibule and the state of the mucosal vasculature both influence maximum flow through the nose; under optimal conditions, nasal flow capacity is close to that via the mouth.     

Effects of expiratory loading on respiration in humans

We examined the effects of expiratory resistive loads of 10 and 18 cmH2O.l-1.s in healthy subjects on ventilation and occlusion pressure responses to CO2, respiratory muscle electromyogram, pattern of breathing, and thoracoabdominal movements. In addition, we compared ventilation and occlusion pressure responses to CO2 breathing elicited by breathing through an inspiratory resistive load of 10 cmH2O.l-1.s to those produced by an expiratory load of similar magnitude. Both inspiratory and expiratory loads decreased ventilatory responses to CO2 and increased the tidal volume achieved at any given level of ventilation. Depression of ventilatory responses to Co2 was greater with the larger than with the smaller expiratory load, but the decrease was in proportion to the difference in the severity of the loads. Occlusion pressure responses were increased significantly by the inspiratory resistive load but not by the smaller expiratory load. However, occlusion pressure responses to CO2 were significantly larger with the greater expiratory load than control. Increase in occlusion pressure observed could not be explained by changes in functional residual capacity or chemical drive. The larger expiratory load also produced significant increases in electrical activity measured during both inspiration and expiration. These results suggest that sufficiently severe impediments to breathing, even when they are exclusively expiratory, can enhance inspiratory muscle activity in conscious humans.     

A hierarchical goal-seeking model of the control of breathing

A model of the overall control of the breathing pattern is presented. The model has the structure of a two-level optimization problem where the lower level criteria determine the shape of the airflow during inspiration and expiration and the higher level criterion determines the values of the other control variables. The model's general formulation makes it possible to obtain predictions of far greater accuracy than before because the previous restrictive assumptions have been avoided by increasing the number of independent control variables. In this model the control variables are the inspiratory time, expiratory time, duration of the end expiratory pause, change in the end expiratory lung volume, the dead space volume, the tidal volume, and the airflow pattern during the cycle. The model's optimization problem has clear and unique minima with respect to each control variable over a wide range of parameter values. Thus the model can be used to predict the effects of various environmental changes.