Activation of the parasternal intercostals during breathing efforts in human subjects

We have tested the possibility that the electromyographic (EMG) activity present in the parasternal intercostal muscles during quiet inspiration was reflexive, rather than agonistic, in nature. Using concentric needle electrodes we measured parasternal EMG activity in four normal subjects during various inspiratory maneuvers. We found that 1) phasic inspiratory activity was invariably present in the parasternal intercostals during quiet breathing, 2) the parasternal EMG activity was generally increased during attempts to perform the tidal breathing maneuver with the diaphragm alone, 3) parasternal EMG activity was markedly decreased or suppressed in the presence of rib cage distortion during diaphragmatic isovolume maneuvers, and 4) that EMG activity could not be voluntarily suppressed during breathing unless the inspired volume was trivial. We conclude that the parasternal EMG activity detected during quiet inspiration in the normal subjects depends on a central involuntary mechanism and is not related to activation of intercostal mechanoreceptors.     

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.     

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.     

Respiratory changes in parasternal intercostal intramuscular pressure

In an attempt to obtain insight in the forces developed by the parasternal intercostal muscles during breathing, changes in parasternal intramuscular pressure (PIP) were measured in 14 supine anesthetized dogs using a microtransducer method. In six animals, during bilateral parasternal stimulation a linear relationship between contractile force exerted on the rib and PIP was demonstrated (r greater than 0.95). In eight animals, during quiet active inspiration, substantial (55 +/- 11.5 cmH2O) PIP was developed. During inspiratory resistive loading and airway occlusion the inspiratory rise in PIP increased in proportion to the inspiratory fall in pleural pressure (r = 0.82). Phrenicotomy and vagotomy resulted in an increase in the inspiratory rise in PIP of 21% and 99%, respectively. During passive deflation, when the parasternal intercostals were passively lengthened, large rises (320 +/- 221 cmH2O) in intramuscular pressure were observed. During passive inflation intramuscular pressure remained constant or even decreased slightly (-8 +/- 25 cmH2O) as expected on the basis of the passive shortening of the muscles. PIP thus invariably increased when tension increased either actively or passively. From PIP it is clear that the parasternals exert significant forces on the ribs during respiratory maneuvers.     

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.     

Mechanics of the parasternal intercostals during occluded breaths in dogs

The electrical activity and the respiratory changes in length of the third parasternal intercostal muscle were measured during single-breath airway occlusion in 12 anesthetized, spontaneously breathing dogs in the supine posture. During occluded breaths in the intact animal, the parasternal intercostal was electrically active and shortened while pleural pressure fell. In contrast, after section of the third intercostal nerve at the chondrocostal junction and abolition of parasternal electrical activity, the muscle always lengthened. This inspiratory muscle lengthening must be related to the fall in pleural pressure; it was, however, approximately 50% less than the amount of muscle lengthening produced, for the same fall in pleural pressure, by isolated stimulation of the phrenic nerves. These results indicate that 1) the parasternal inspiratory shortening that occurs during occluded breaths in the dog results primarily from the muscle inspiratory contraction per se, and 2) other muscles of the rib cage, however, contribute to this parasternal shortening by acting on the ribs or the sternum. The present studies also demonstrate the important fact that the parasternal inspiratory contraction in the dog is really agonistic in nature.     

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.     

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.     

Parasternal and external intercostal responses to various respiratory maneuvers.

Recent studies suggest that the external intercostal (EI) muscles of the upper rib cage, like the parasternals (PA), play an important ventilatory role, even during eupneic breathing. The purpose of the present study was to further assess the ventilatory role of the EI muscles by determining their response to various static and dynamic respiratory maneuvers and comparing them with the better-studied PA muscles. Applied interventions included 1) passive inflation and deflation, 2) abdominal compression, 3) progressive hypercapnia, and 4) response to bilateral cervical phrenicotomy. Studies were performed in 11 mongrel dogs. Electromyographic (EMG) activities were monitored via bipolar stainless steel electrodes. Muscle length (percentage of resting length) was monitored with piezoelectric crystals. With passive rib cage inflation produced either with a volume syringe or abdominal compression, each muscle shortened; with passive deflation, each muscle lengthened. During eupneic breathing, each muscle was electrically active and shortened to a similar degree. In response to progressive hypercapnia, peak EMG of each intercostal muscle increased linearly and to a similar extent. Inspiratory shortening also increased progressively with increasing PCO2, but in a curvilinear fashion with no significant differences in response among intercostal muscles. In response to phrenicotomy, the EMG and degree of inspiratory shortening of each intercostal muscle increased significantly. Again, the response among intercostal muscles was not significantly different.(ABSTRACT TRUNCATED AT 250 WORDS)     

Relationship between parasternal intercostal length and rib cage displacement in dogs

The relationship between parasternal intercostal length and rib cage cross-sectional area was examined in nine supine dogs during passive inflation and during quiet breathing before and after phrenicotomy. Parasternal intercostal length (PSL) was measured with a sonomicrometry technique, and rib cage cross-sectional area (Arc) was measured with a Respitrace coil placed around the middle rib cage. During active inspiration as well as during passive inflation, PSL decreased as Arc increased. However, the relationship between PSL and Arc during active inspiration, whether in the intact or phrenicotomized animal, was almost invariably different from that during passive inflation, so that the same increase in Arc was associated with a greater decrease in PSL in the former than in the latter instance. This difference between passive inflation and active inspiration is probably due to the active contraction of the parasternals during inspiration and the consequent caudal displacement of the sternum. In upright humans, the sternum moves cephalad and not caudad during inspiration, so the relationship between PSL and Arc during active breathing might be similar to that during passive inflation.     

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.     

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%.     

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.     

Effects of tracheal airway occlusion on hyoid muscle length and upper airway volume

Complex relationships exist among electromyograms (EMGs) of the upper airway muscles, respective changes in muscle length, and upper airway volume. To test the effects of preventing lung inflation on these relationships, recordings were made of EMGs and length changes of the geniohyoid (GH) and sternohyoid (SH) muscles as well as of tidal changes in upper airway volume in eight anesthetized cats. During resting breathing, tracheal airway occlusion tended to increase the inspiratory lengthening of GH and SH. In response to progressive hypercapnia, the GH eventually shortened during inspiration in all animals; the extent of muscle shortening was minimally augmented by airway occlusion despite substantial increases in EMGs. SH lengthened during inspiration in six of eight animals under hypercapnic conditions, and in these cats lengthening was greater during airway occlusion even though EMGs increased. Despite the above effects on SH and GH length, upper airway tidal volume was increased significantly by tracheal occlusion under hypercapnic conditions. These data suggest that the thoracic and upper airway muscle reflex effects of preventing lung inflation during inspiration act antagonistically on hyoid muscle length, but, because of the mechanical arrangement of the hyoid muscles relative to the airway and thorax, they act agonistically to augment tidal changes in upper airway volume. The augmentation of upper airway tidal volume may occur in part as a result of the effects of thoracic movements being passively transmitted through the hyoid muscles.     

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.     

Voluntary hyperventilation changes recruitment order of parasternal intercostal motor units

The order of recruitment of single-motor units in parasternal intercostal muscles during inspiration was studied in normal human subjects during quiet breathing and voluntary hyperventilation. Electromyograms were recorded from the second and third intercostal spaces by means of bipolar fine wire electrodes. Flow at the mouth, volume, end-expired CO2, and rib cage and abdominal anterior-posterior diameters were monitored. Single-motor units were identified using criteria of amplitude and shape, and the time of first appearance of each unit in each inspiration was noted. Hyperventilation was performed with visual feedback of the display of rib cage and abdomen excursions, keeping the ratio of rib cage to abdominal expansion. Subjects were normocapnic in quiet breathing and developed hypocapnia during hyperventilation. Recruitment order was stable in quiet breathing, but in some cases was altered during voluntary hyperventilation. Some low threshold units that fired early in the breath in quiet breathing fired earlier at the beginning of a period of voluntary hyperventilation but progressively later in the breath as hyperventilation went on, whereas later firing units moved progressively toward the early part of inspiration. This suggests that different groups of motoneurons in the pool supplying parasternal intercostal muscles receive different patterns of synaptic input.     

Patterns of intercostal muscle activity in humans

Coordination of activity of inspiratory intercostal muscles in conscious human subjects was studied by means of an array of electromyograph (EMG) electrodes. Bipolar fine wire electrodes were placed in the second and fourth parasternal intercostal muscles and in two or three external intercostal muscles in the midaxillary line from the fourth to eighth intercostal spaces. Subjects breathed quietly or rebreathed from a bag containing 8% CO2 in O2 in both supine and upright postures. Respiration was monitored by means of flow, volume, and separate rib cage and abdominal volumes. Onset of EMG activity in each breath was found near the beginning of inspiration in the uppermost intercostal spaces but progressively later in inspiration in lower spaces, indicating that activity spreads downward across the rib cage through inspiration. At higher ventilation stimulated by CO2, activity spread further and faster downward. In voluntary deep breathing, external intercostal muscles tended to be recruited earlier in inspiration than in CO2-stimulated breathing. The change from supine to sitting resulted in small and inconsistent changes. There was no lung volume or rib cage volume threshold for appearance of EMG activity in any of the spaces.     

Passive mechanics of upright human chest wall during immersion from hips to neck

We have determined the mechanical effects of immersion to the neck on the passive chest wall of seated upright humans. Repeated measurements were made at relaxed end expiration on four subjects. Changes in relaxed chest wall configuration were measured using magnetometers. Gastric and esophageal pressures were measured with balloon-tipped catheters in three subjects; from these, transdiaphragmatic pressure was calculated. Transabdominal pressure was estimated using a fluid-filled, open-tipped catheter referenced to the abdomen's exterior vertical surface. We found that immersion progressively reduced mean transabdominal pressure to near zero and that the relaxed abdominal wall was moved inward 3-4 cm. The viscera were displaced upward into the thorax, gastric pressure increased by 20 cmH2O, and transdiaphragmatic pressure decreased by 10-15 cmH2O. This lengthened the diaphragm, elevating the diaphragmatic dome 3-4 cm. Esophageal pressure became progressively more positive throughout immersion, increasing by 8 cmH2O. The relaxed rib cage was elevated and expanded by raising water from hips to lower sternum; this passively shortened the inspiratory intercostals and the accessory muscles of inspiration. Deeper immersion distorted the thorax markedly: the upper rib cage was forced inward while lower rib cage shape was not systematically altered and the rib cage remained elevated. Such distortion may have passively lengthened or shortened the inspiratory muscles of the rib cage, depending on their location. We conclude that the nonuniform forcing produced by immersion provides unique insights into the mechanical characteristics of the abdomen and rib cage, that immersion-induced length changes differ among the inspiratory muscles according to their locations and the depth of immersion, and that such length changes may have implications for patients with inspiratory muscle deficits.     

Electrical and mechanical activity of respiratory muscles during hypercapnia

In nine anesthetized supine spontaneously breathing dogs, we compared moving average electromyograms (EMGs) of the costal diaphragm and the third parasternal intercostal muscles with their respective respiratory changes in length (measured by sonomicrometry). During resting O2 breathing the pattern of diaphragm and intercostal muscle inspiratory shortening paralleled the gradually incrementing pattern of their moving average EMGs. Progressive hypercapnia caused progressive increases in the amount and velocity of respiratory muscle inspiratory shortening. For both muscles there were linear relationships during the course of CO2 rebreathing between their peak moving average EMGs and total inspiratory shortening and between tidal volume and total inspiratory shortening. During single-breath airway occlusions, the electrical activity of both the diaphragm and intercostal muscles increased, but there were decreases in their tidal shortening. The extent of muscle shortening during occluded breaths was increased by hypercapnia, so that both muscles shortened more during occluded breaths under hypercapnic conditions (PCO2 up to 90 Torr) than during unoccluded breaths under normocapnic conditions. These results suggest that for the costal diaphragm and parasternal intercostal muscles there is a close relationship between their electrical and mechanical behavior during CO2 rebreathing, this relationship is substantially altered by occluding the airway for a single breath, and thoracic respiratory muscles do not contract quasi-isometrically during occluded breaths.     

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.