Synergism between the canine left and right hemidiaphragms.

Expansion of the lung during inspiration results from the coordinated contraction of the diaphragm and several groups of rib cage muscles, and we have previously shown that the changes in intrathoracic pressure generated by the latter are essentially additive. In the present studies, we have assessed the interaction between the right and left hemidiaphragms in anesthetized dogs by comparing the changes in airway opening pressure (DeltaPao) obtained during simultaneous stimulation of the two phrenic nerves (measured DeltaPao) to the sum of the DeltaPao values produced by their separate stimulation (predicted DeltaPao). The measured DeltaPao was invariably greater than the predicted DeltaPao, and the ratio between these two values increased gradually as the stimulation frequency was increased; the ratio was 1.10 +/- 0.01 (P < 0.05) for a frequency of 10 Hz, whereas for a frequency of 50 Hz it amounted to 1.49 +/- 0.05 (P < 0.001). This interaction remained unchanged after the rib cage was stiffened and its compliance was made linear, thus indicating that the load against which the diaphragm works is not a major determinant. However, radiographic measurements showed that stimulation of one phrenic nerve extends the inactive hemidiaphragm toward the sagittal midplane and reduces the caudal displacement of the central portion of the diaphragmatic dome. As a result, the volume swept by the contracting hemidiaphragm is smaller than the volume it displaces when the contralateral hemidiaphragm also contracts. These observations indicate that 1) the left and right hemidiaphragms have a synergistic, rather than additive, interaction on the lung; 2) this synergism operates already during quiet breathing and increases in magnitude when respiratory drive is greater; and 3) this synergism is primarily related to the configuration of the muscle.     

Rib cage muscle interaction in airway pressure generation

We have previously demonstrated in dogs that the change inairway opening pressure (Pao) produced by isolated maximumactivation of the parasternal intercostal or triangularis sterni musclein a single interspace, the sternomastoids, and the scalenes isproportional to the product of muscle mass and the fractional change inmuscle length per unit volume increase of the relaxed chest wall. In the present study, we have assessed the interactions between these muscles by comparing the Pao obtained during simultaneous activation of a pair of muscles (measured Pao) to the sum of the Pao values obtained during their separate activation (predicted Pao). Measured and predicted Pao values were compared for the following pairs ofmuscles: the parasternal intercostals in two interspaces, the parasternal intercostals in one interspace and either thesternomastoids or the scalenes, two segments of the triangularissterni, and the interosseous intercostals in two contiguousinterspaces. For all these pairs, the measured Pao was within~10% of the predicted value. We therefore conclude that1) the pressure changes generated bythe rib cage muscles are essentially additive; and2) measurements of the mass of aparticular muscle and of its fractional change in length during passiveinflation can be used to estimate the potential pressure-generatingability of the muscle during coordinated activity as well as duringisolated activation.

     

Respiratory function of intercostal muscles in supine dog: an electromyographic study

It is traditionally considered that the difference in orientation of the muscle fibers makes the external intercostals elevate the ribs and the internal interosseous intercostals lower the ribs during breathing. This traditional view, however, has recently been challenged by the observation that the external and internal interosseous intercostals, when contracting alone in a single interspace, have a similar effect on the ribs into which they insert. This view has also been challenged by the observation that the external and internal intercostals in a given interspace often change their length in the same direction during breathing. In an attempt to clarify the respiratory function of these muscles, we studied eight supine lightly anesthetized dogs during quiet breathing and during static inspiratory efforts. In each animal electromyographic (EMG) recordings from the external and internal interosseous intercostals were obtained in all interspaces from the second to the eighth, and selective denervations were systematically performed to ensure with complete certainty the origin of the recorded EMG activities. The external intercostals were only activated in phase with inspiration, whereas the internal interosseous intercostals were only activated in phase with expiration. These phasic EMG activities, however, were generally small in magnitude, and the muscles were often silent. Indeed, activation of the externals was always confined to the upper portion of the rib cage, whereas activation of the internals was limited to the lower portion of the rib cage. Internal intercostal activation always occurred sequentially along a caudocephalic gradient. These observations are thus compatible with the traditional view of intercostal muscle action.(ABSTRACT TRUNCATED AT 250 WORDS)     

Respiratory changes in parasternal intercostal length

In an attempt to understand the role of the parasternal intercostals in respiration, we measured the changes in length of these muscles during a variety of static and dynamic respiratory maneuvers. Studies were performed on 39 intercostal spaces from 10 anesthetized dogs, and changes in parasternal intercostal length were assessed with pairs of piezoelectric crystals (sonomicrometry). During static maneuvers (passive inflation-deflation, isovolume maneuvers, changes in body position), the parasternal intercostals shortened whenever the rib cage inflated, and they lengthened whenever the rib cage contracted. The changes in parasternal intercostal length, however, were much smaller than the changes in diaphragmatic length, averaging 9.2% of the resting length during inflation from residual volume to total lung capacity and 1.3% during tilting from supine to upright. During quiet breathing the parasternal intercostals always shortened during inspiration and lengthened during expiration. In the intact animals the inspiratory parasternal shortening was close to that seen for the same increase in lung volume during passive inflation and averaged 3.5%. After bilateral phrenicotomy, however, the parasternal intercostal shortening during inspiration markedly increased, whereas tidal volume diminished. These results indicate that 1) the parasternal intercostals in the dog are real agonists (as opposed to fixators) and actively contribute to expand the rib cage and the lung during quiet inspiration, 2) the relationship between lung volume and parasternal length is not unique but depends on the relative contribution of the various inspiratory muscles to tidal volume, and 3) the physiological range of operating length of the parasternal intercostals is considerably smaller than that of the diaphragm.(ABSTRACT TRUNCATED AT 250 WORDS)     

Inspiratory function of the levator costae and external intercostal muscles in the dog

The shortening of the canine parasternal intercostals during inspiration may have a passive component, and we have previously speculated that this might result from the actions of the levator costae and external intercostals (J. Appl. Physiol. 66: 1421-1429, 1989). The present studies were designed, therefore, to evaluate the pattern of activation of these muscles in the dog and to define their action on the rib cage during breathing. The results indicate that 1) the levator costae and external intercostals in the cranial part of the rib cage are active during inspiration, both in the supine and in the prone posture; 2) the inspiratory activation of the two muscles is increased after bilateral phrenicotomy; 3) it is increased even more when the parasternal intercostals in the different interspaces are also denervated; and 4) when the levator costae and external intercostals are the only muscles active during inspiration, the ribs continue to move cranially, and the sternum, rather than moving caudally as it does in the intact animal, moves cranially as well. Therefore, we conclude that the levator costae and external intercostals in the dog have a true inspiratory function. When needed, they are capable of causing a significant expansion of the rib cage and the lung during breathing.     

Passive shortening of canine parasternal intercostals during breathing

We have previously demonstrated that the shortening of the canine parasternal intercostals during inspiration results primarily from the muscles' own activation (J. Appl. Physiol. 64: 1546-1553, 1988). In the present studies, we have tested the hypothesis that other inspiratory rib cage muscles may contribute to the parasternal inspiratory shortening. Eight supine, spontaneously breathing dogs were studied. Changes in length of the third or fourth right parasternal intercostal were measured during quiet breathing and during single-breath airway occlusion first with the animal intact, then after selective denervation of the muscle, and finally after bilateral phrenicotomy. Denervating the parasternal virtually eliminated the muscle shortening during quiet inspiration and caused the muscle to lengthen during occluded breaths. After phrenicotomy, however, the parasternal, while being denervated, shortened again a significant amount during both quiet inspiration and occluded breaths. These data thus confirm that a component of the parasternal inspiratory shortening is not active and results from the action of other inspiratory rib cage muscles. Additional studies in four animals demonstrated that the scalene and serratus muscles do not play any role in this phenomenon; it must therefore result from the action of intrinsic rib cage muscles.     

On the respiratory function of the ribs.

To assess the respiratory function of the ribs, we measured the changes in airway opening pressure (Pao) induced by stimulation of the parasternal and external intercostal muscles in anesthetized dogs, first before and then after the bony ribs were removed from both sides of the chest. Stimulating either set of muscles with the rib cage intact elicited a fall in Pao in all animals. After removal of the ribs, however, the fall in Pao produced by the parasternal intercostals was reduced by 60% and the fall produced by the external intercostals was eliminated. The normal outward curvature of the rib cage was also abolished in this condition, and when the curvature was restored by a small inflation, external intercostal stimulation consistently elicited a rise rather than a fall in Pao. These findings thus confirm that the ribs play a critical role in the act of breathing by converting intercostal muscle shortening into lung volume expansion. In addition, they carry the compression that is required to balance the pressure difference across the chest wall.     

Respiratory effects of the scalene and sternomastoid muscles in humans.

Previous studies have shown that in normal humans the change in airway opening pressure (DeltaPao) produced by all the parasternal and external intercostal muscles during a maximal contraction is approximately -18 cmH(2)O. This value is substantially less negative than DeltaPao values recorded during maximal static inspiratory efforts in subjects with complete diaphragmatic paralysis. In the present study, therefore, the respiratory effects of the two prominent inspiratory muscles of the neck, the sternomastoids and the scalenes, were evaluated by application of the Maxwell reciprocity theorem. Seven healthy subjects were placed in a computed tomographic scanner to determine the fractional changes in muscle length during inflation from functional residual capacity to total lung capacity and the masses of the muscles. Inflation induced greater shortening of the scalenes than the sternomastoids in every subject. The inspiratory mechanical advantage of the scalenes thus averaged (mean +/- SE) 3.4 +/- 0.4%/l, whereas that of the sternomastoids was 2.0 +/- 0.3%/l (P < 0.001). However, sternomastoid muscle mass was much larger than scalene muscle mass. As a result, DeltaPao generated by a maximal contraction of either muscle would be 3-4 cmH(2)O, which is about the same as DeltaPao generated by the parasternal intercostals in all interspaces.     

Coupling between triangularis sterni and parasternals during breathing in dogs

The purpose of the present studies was to assess the functional coupling between the parasternal intercostals and the triangularis sterni (transversus thoracis) muscles during resting breathing, and we measured the electrical activity and the respiratory changes in length of these two muscles in 13 supine anesthetized dogs. The changes in muscle length were defined relative to their respective in situ relaxation length (Lr). During inspiration, the parasternal intercostals were active and shortened below Lr, causing the triangularis sterni to be passively stretched above Lr. Shortly after the cessation of parasternal contraction, the triangularis sterni became active and shortened below Lr, and in nine animals this active shortening was associated with a forcible distension of the parasternal intercostals above Lr. Deactivation of the triangularis sterni at end expiration caused both muscles to return to their respective Lr. This pattern was essentially unchanged after supplemental anesthesia and bilateral phrenicotomy. We conclude that in dogs breathing quietly the length of the rib cage muscles during the expiratory pause is not passively determined as conventionally thought.     

Interaction between the canine diaphragm and intercostal muscles in lung expansion.

Changes in intrathoracic pressure produced by the various inspiratory intercostals are essentially additive, but the interaction between these muscles and the diaphragm remains uncertain. In the present study, this interaction was assessed by measuring the changes in airway opening (DeltaPao) or transpulmonary pressure (DeltaPtp) in vagotomized, phrenicotomized dogs during spontaneous inspiration (isolated intercostal contraction), during isolated rectangular or ramp stimulation of the peripheral ends of the transected C(5) phrenic nerve roots (isolated diaphragm contraction), and during spontaneous inspiration with superimposed phrenic nerve stimulation (combined diaphragm-intercostal contraction). With the endotracheal tube occluded at functional residual capacity, DeltaPao during combined diaphragm-intercostal contraction was nearly equal to the sum of the DeltaPao produced by the two muscle groups contracting individually. However, when the endotracheal tube was kept open, DeltaPtp during combined contraction was 123% of the sum of the individual DeltaPtp (P < 0.001). The increase in lung volume during combined contraction was also 109% of the sum of the individual volume increases (P < 0.02). Abdominal pressure during combined contraction was invariably lower than during isolated diaphragm contraction. It is concluded, therefore, that the canine diaphragm and intercostal muscles act synergistically during lung expansion and that this synergism is primarily due to the fact that the intercostal muscles reduce shortening of the diaphragm. When the lung is maintained at functional residual capacity, however, the synergism is obscured because the greater stiffness of the rib cage during diaphragm contraction enhances the DeltaPao produced by the isolated diaphragm and reduces the DeltaPao produced by the intercostal muscles.     

Mechanical arrangement of the parasternal intercostals in the different interspaces

When the parasternal intercostal in a single interspace is selectively denervated in dogs with diaphragmatic paralysis, it continues to shorten during both quiet and occluded inspiration. In the present studies, we have tested the hypothesis that this passive parasternal inspiratory shortening is due to the action of the other parasternal intercostals. Changes in length of the denervated third right parasternal were measured in eight supine phrenicotomized animals. We found that 1) the inspiratory muscle shortening increased after denervation of the third left parasternal but gradually decreased with denervation of the parasternals situated in the second, fourth, and fifth interspaces; 2) the muscle, however, always continued to shorten during inspiration, even after denervation of all the parasternals; 3) stimulating selectively the third left parasternal caused a muscle lengthening; and 4) bilateral stimulation of the parasternals in the second or the fourth interspace produced a muscle shortening. We conclude that 1) the two parasternals situated in the same interspace on both sides of the sternum are mechanically arranged in series, whereas the parasternals located in adjacent interspaces are mechanically arranged in parallel; and 2) if a denervated parasternal continues to shorten during inspiration, this is in part because of the action of the parasternals in the adjacent interspaces and in part because of other inspiratory muscles of the rib cage, possibly the external intercostals and the levator costae.     

Linkage between parasternals and external intercostals during resting breathing

To assess the mechanical coupling between the parasternal and external intercostals in the cranial portion of the rib cage, we measured the respiratory changes in length and the electromyograms of the two muscles in the same third or fourth intercostal space in 24 spontaneously breathing dogs. We found that 1) the amount of inspiratory shortening of the external intercostal was considerably smaller than the amount of shortening of the parasternal; 2) after selective denervation of the parasternal, the inspiratory shortening of both the parasternal and the external intercostal was almost abolished; 3) on the other hand, after selective denervation of the external intercostal, the inspiratory shortening of the parasternal was unchanged, and the inspiratory shortening of the external intercostal was reduced but not suppressed; and 4) this persistent shortening of the external intercostal was reversed into a clear-cut inspiratory lengthening when the parasternal was subsequently denervated. We conclude that in the dog 1) the inspiratory contraction of the external intercostals in the cranial portion of the rib cage is agonistic in nature as is the contraction of the parasternals; 2) during resting breathing, however, the changes in length of these external intercostals are largely determined by the action of the parasternals. These observations are consistent with the idea that in the dog, the parasternals play a larger role than the external intercostals in elevating the ribs during resting inspiration.     

Rib cage shape and motion in microgravity.

We studied the effect of microgravity (0 Gz) on the anteroposterior diameters of the upper (URC-AP) and lower (LRC-AP) rib cage, the transverse diameter of the lower rib cage (LRC-TR), and the xiphipubic distance and on the electromyographic (EMG) activity of the scalene and parasternal intercostal muscles in five normal subjects breathing quietly in the seated posture. Gastric pressure was also recorded in four subjects. At 0 Gz, end-expiratory LRC-AP and xiphipubic distance increased but LRC-TR invariably decreased, as did end-expiratory gastric pressure. No consistent effect was observed on tidal LRC-TR and xiphipubic displacements, but tidal changes in URC-AP and LRC-AP were reduced. Although scalene and parasternal phasic inspiratory EMG activity tended to decrease at 0 Gz, both muscle groups demonstrated an increase in tonic activity. We conclude that during brief periods of weightlessness 1) the rib cage at end expiration is displaced in the cranial direction and adopts a more circular shape, 2) the tidal expansion of the ventral rib cage is reduced, particularly in its upper portion, and 3) the scalenes and parasternal intercostals generally show a decrease in phasic inspiratory EMG activity and an increase in tonic activity.     

Action of intercostal muscles on the lung in dogs

The action on the lung of interosseous intercostal muscles located in the third and the seventh interspaces was studied in 15 anesthetized-curarized supine dogs. Changes in pleural pressure, airflow rate, and lung volume produced by maximal stimulation of both intercostal muscle layers were measured at and above functional residual capacity (FRC). In five animals measurements were also obtained during isolated stimulation of the internal layer. At FRC, intercostal stimulation in the upper interspaces had invariably an inspiratory effect on the lung but no effect was detectable in the lower interspaces. Qualitatively similar results were obtained during isolated stimulation of the internal layer. Increasing lung volume reduced the inspiratory action of the upper intercostals and conferred an expiratory action to the lower intercostals. These results indicate the following: 1) when contracting in a single interspace, the external and internal intercostals have a qualitatively similar action on the lung; and 2) this action, however, depends critically on their location along the cephalocaudal axis of the rib cage: in the upper portion of the rib cage, both muscle layers have an inspiratory effect at and above FRC; in the lower portion of the rib cage, they have no respiratory action at FRC and act in the expiratory direction at higher lung volumes.     

Inspiratory elevation of the ribs in the dog: primary role of the parasternals

To assess the relative contributions of the different groups of inspiratory intercostal muscles to the cranial motion of the ribs in the dog, we have measured the axial displacement of the fourth rib and recorded the electromyograms of the parasternal intercostal, external intercostal, and levator costae in the third interspace in 15 anesthetized animals breathing at rest. In eight animals, the parasternal intercostals were denervated in interspaces 1-5. This procedure caused a marked increase in the amount of external intercostal and levator costae inspiratory activity, and yet the inspiratory cranial motion of the rib was reduced by 55%. On the other hand, the external intercostals in interspaces 1-5 were sectioned in seven animals, and the reduction in the cranial rib motion was only 22%; the amount of parasternal and levator costae activity, however, was unchanged. When the parasternals in these animals were subsequently denervated, the levator costae inspiratory activity increased markedly, but the inspiratory cranial motion of the rib was abolished or reversed into an inspiratory caudal motion. These studies thus confirm that, in the dog breathing at rest, the parasternal intercostals have a larger role than the external intercostals and levator costae in causing the cranial motion of the ribs during inspiration. A quantitative analysis suggests that the parasternal contribution is approximately 80%.     

Reflex effect of esophageal distension on respiratory muscle activity and pressure

The electrical activity of the respiratory skeletal muscles is altered in response to reflexes originating in the gastrointestinal tract. The present study evaluated the reflex effects of esophageal distension (ED) on the distribution of motor activity to both inspiratory and expiratory muscles of the rib cage and abdomen and the resultant changes in thoracic and abdominal pressure during breathing. Studies were performed in 21 anesthetized spontaneously breathing dogs. ED was produced by inflating a balloon in the distal esophagus. ED decreased the activity of the costal and crural diaphragm and external intercostals and abolished all preexisting electrical activity in the expiratory muscles of the abdominal wall. On the other hand, ED increased the activity of the parasternal intercostals and expiratory muscles located in the rib cage (i.e., triangularis sterni and internal intercostal). All effects of ED were graded, with increasing distension exerting greater effects, and were eliminated by vagotomy. The effect of increases in chemical drive and lung inflation reflex activity on the response to ED was examined by performing ED while animals breathed either 6.5% CO2 or against graded levels of positive end-expiratory pressure (PEEP), respectively. Changes in respiratory muscle electrical activity induced by ED were similar (during 6.5% CO2 and PEEP) to those observed under control conditions. We conclude that activation of mechanoreceptors in the esophagus reflexly alters the distribution of motor activity to the respiratory muscles, inhibiting the muscles surrounding the abdominal cavity and augmenting the parasternals and expiratory muscles of the chest wall.     

Effect of inflation on the interaction between the left and right hemidiaphragms.

At resting end expiration [functional residual capacity (FRC)], the actions of the left and right hemidiaphragms on the lung are synergistic. However, the synergism decreases in magnitude as muscle tension decreases. Therefore, the hypothesis was tested in anesthetized dogs that the degree of synergism between the two hemidiaphragms also decreases with increasing lung volume. In a first experiment, the changes in airway opening pressure (DeltaPao) and abdominal pressure (DeltaPab) obtained during simultaneous stimulation of the left and right phrenic nerves (measured changes in pressure) at different lung volumes were compared with the sum of the pressure changes produced by their separate stimulation (predicted changes in pressure). Although the pressure changes decreased markedly with increasing lung volume, the measured DeltaPao and DeltaPab were substantially greater than the predicted values at all lung volumes. The ratio of the measured to the predicted DeltaPao, in fact, remained constant. In a second experiment, radiographic measurements showed that the fractional shortening of the muscle during bilateral contraction at high lung volumes was similar to that during unilateral contraction. During unilateral contraction at high lung volumes, however, the passive hemidiaphragm moved in the cranial direction, whereas, during unilateral contraction at FRC, it moved in the caudal direction. These observations indicate that 1) for a given muscle tension, the synergism between the two halves of the diaphragm is greater at high lung volumes than at FRC; and 2) this difference is primarily related to the greater distortion of the muscle configuration.     

The effect of lung inflation on the inspiratory action of the canine parasternal intercostals.

Inflation induces a marked decrease in the lung-expanding ability of the diaphragm, but its effect on the parasternal intercostal muscles is uncertain. To assess this effect, the phrenic nerves and the external intercostals were severed in anesthetized, vagotomized dogs, such that the parasternal intercostals were the only muscles active during inspiration, and the endotracheal tube was occluded at different lung volumes. Although the inspiratory electromyographic activity recorded from the muscles was constant, the change in airway opening pressure decreased with inflation from -7.2+/-0.6 cmH2O at functional residual capacity to -2.2+/-0.2 cmH2O at 20-cmH2O transrespiratory pressure (P<0.001). The inspiratory cranial displacement of the ribs remained virtually unchanged, and the inspiratory caudal displacement of the sternum decreased moderately. However, the inspiratory outward rib displacement decreased markedly and continuously; at 20 cmH2O, this displacement was only 23+/-2% of the value at functional residual capacity. Calculations based on this alteration yielded substantial decreases in the change in airway opening pressure. It is concluded that, in the dog, 1) inflation affects adversely the lung-expanding actions of both the parasternal intercostals and the diaphragm; and 2) the adverse effect of inflation on the parasternal intercostals is primarily related to the alteration in the kinematics of the ribs. As a corollary, it is likely that hyperinflation also has a negative impact on the parasternal intercostals in patients with chronic obstructive pulmonary disease.     

Effect of diaphragmatic contraction on the action of the canine parasternal intercostals.

The inspiratory intercostal muscles enhance the force generated by the diaphragm during lung expansion. However, whether the diaphragm also alters the force developed by the inspiratory intercostals is unknown. Two experiments were performed in dogs to answer the question. In the first experiment, external, cranially oriented forces were applied to the different rib pairs to assess the effect of diaphragmatic contraction on the coupling between the ribs and the lung. The fall in airway opening pressure (deltaPa(O)) produced by a given force on the ribs was invariably greater during phrenic nerve stimulation than with the diaphragm relaxed. The cranial rib displacement (Xr), however, was 40-50% smaller, thus indicating that the increase in deltaPa(O) was exclusively the result of the increase in diaphragmatic elastance. In the second experiment, the parasternal intercostal muscle in the fourth interspace was selectively activated, and the effects of diaphragmatic contraction on the deltaPa(O) and Xr caused by parasternal activation were compared with those observed during the application of external loads on the ribs. Stimulating the phrenic nerves increased the deltaPa(O) and reduced the Xr produced by the parasternal intercostal, and the magnitudes of the changes were identical to those observed during external rib loading. It is concluded, therefore, that the diaphragm has no significant synergistic or antagonistic effect on the force developed by the parasternal intercostals during breathing. This lack of effect is probably related to the constraint imposed on intercostal muscle length by the ribs and sternum.     

Action of human respiratory muscles inferred from finite element analysis of rib cage.

The actions of several human respiratory muscles have been inferred from finite element analysis of the rib cage. The human model is based on anatomic and mechanical measurements in dogs and human cadavers. As in an earlier canine model, the external and internal (interosseous) intercostal muscles were found to cause, respectively, inspiratory and expiratory displacements of the rib cage, in agreement with the two-dimensional geometric analysis of Hamberger. When extended to three dimensions, Hamberger's analysis helps explain why muscles at the side of the rib cage produce changes in the anteroposterior diameter, whereas muscles at the front and back of the rib cage cause changes in the transverse diameter.