Postinspiratory activity of the parasternal and external intercostal muscles in awake canines.

Previous studies have shown in awake dogs that activity in the crural diaphragm, but not in the costal diaphragm, usually persists after the end of inspiratory airflow. It has been suggested that this difference in postinspiratory activity results from greater muscle spindle content in the crural diaphragm. To evaluate the relationship between muscle spindles and postinspiratory activity, we have studied the pattern of activation of the parasternal and external intercostal muscles in the second to fourth interspaces in eight chronically implanted animals. Recordings were made on 2 or 3 successive days with the animals breathing quietly in the lateral decubitus position. The two muscles discharged in phase with inspiration, but parasternal intercostal activity usually terminated with the cessation of inspiratory flow, whereas external intercostal activity persisted for 24.7 +/- 12.3% of inspiratory time (P < 0.05). Forelimb elevation in six animals did not affect postinspiratory activity in the parasternal but prolonged postinspiratory activity in the external intercostal to 45.4 +/- 16.3% of inspiratory time (P < 0.05); in two animals, activity was still present at the onset of the next inspiratory burst. These observations support the concept that muscle spindles are an important determinant of postinspiratory activity. The absence of such activity in the parasternal intercostals and costal diaphragm also suggests that the mechanical impact of postinspiratory activity on the respiratory system is smaller than conventionally thought.     

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.     

Gas exchange during separate diaphragm and intercostal muscle breathing.

In patients with diaphragm paralysis, ventilation to the basal lung zones is reduced, whereas in patients with paralysis of the rib cage muscles, ventilation to the upper lung zones in reduced. Inspiration produced by either rib cage muscle or diaphragm contraction alone, therefore, may result in mismatching of ventilation and perfusion and in gas-exchange impairment. To test this hypothesis, we assessed gas exchange in 11 anesthetized dogs during ventilation produced by either diaphragm or intercostal muscle contraction alone. Diaphragm activation was achieved by phrenic nerve stimulation. Intercostal muscle activation was accomplished by electrical stimulation by using electrodes positioned epidurally at the T(2) spinal cord level. Stimulation parameters were adjusted to provide a constant tidal volume and inspiratory flow rate. During diaphragm (D) and intercostal muscle breathing (IC), mean arterial Po(2) was 97.1 +/- 2.1 and 88.1 +/- 2.7 Torr, respectively (P < 0.01). Arterial Pco(2) was lower during D than during IC (32.6 +/- 1.4 and 36.6 +/- 1.8 Torr, respectively; P < 0.05). During IC, oxygen consumption was also higher than that during D (0.13 +/- 0.01 and 0.09 +/- 0.01 l/min, respectively; P < 0.05). The alveolar-arterial oxygen difference was 11.3 +/- 1.9 and 7.7 +/- 1.0 Torr (P < 0.01) during IC and D, respectively. These results indicate that diaphragm breathing is significantly more efficient than intercostal muscle breathing. However, despite marked differences in the pattern of inspiratory muscle contraction, the distribution of ventilation remains well matched to pulmonary perfusion resulting in preservation of normal gas exchange.     

Parasternal and external intercostal muscle shortening during eupneic breathing

The interosseous external intercostal (EI) muscles of the upper rib cage are electrically active during inspiration, but the mechanical consequence of their activation is unclear. In 16 anesthetized dogs, we simultaneously measured EI (3rd and 4th interspaces) and parasternal intercostal (PA) (3rd interspace) electromyogram and length. Muscle length was measured by sonomicrometry and expressed as a percentage of resting length (%LR). During resting breathing, each muscle was electrically active and shortened to a similar extent. Sequential EI muscle denervation (3rd and 4th interspaces) followed by PA denervation (3rd interspace) demonstrated significant reductions in the degree of inspiratory shortening for each muscle. Mean EI muscle shortening of the third and fourth interspaces decreased from -3.4 +/- 0.5 and -3.0 +/- 0.4% LR (SE) under control conditions to -0.2 +/- 0.2 and -0.8 +/- 0.3% LR, respectively, after selective denervation of each of these muscles (P less than 0.001 for each). After selective denervation of the PA muscle, its shortening decreased from -3.5 +/- 0.3 to +0.6% LR (SE) (P less than 0.001). PA muscle denervation also caused the EI muscle in the third interspace to change from inspiratory shortening of -0.2% to inspiratory lengthening of +0.2% +/- 0.2 (P less than 0.05). We conclude that during eupneic breathing 1) the EI muscles of the upper rib cage, like the PA muscles, are inspiratory agonists and actively contribute to rib cage expansion and 2) PA muscle contraction contributes to EI muscle shortening.     

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.     

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.     

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.     

The two mechanisms of intercostal muscle action on the lung.

The mechanisms of respiratory action of the intercostal muscles were studied by measuring the effect of external forces (F) applied to the ribs and by modeling the effect of F exerted by the intercostal muscles. In five dogs, with the airway occluded, cranial F were applied to individual rib pairs, from the 2nd to the 11th rib pair, and the change in airway opening pressure (Pao) was measured. The ratio Pao/F increases with increasing rib number in the upper ribs (2nd to 5th) and decreases in the lower ribs (5th to 11th). These data were incorporated into a model for the geometry of the ribs and intercostal muscles, and Pao/F was calculated from the model. For interspaces 2-8, the calculated values agree reasonably well with previously measured values. From the modeling, two mechanisms of intercostal muscle action are identified. One is the well-known Hamberger mechanism, modified to account for the three-dimensional geometry of the rib cage. This mechanism depends on the slant of an intercostal muscle relative to the ribs and on the resulting difference between the moments applied to the upper and lower ribs that bound each interspace. The second is a new mechanism that depends on the difference between the values of Pao/F for the upper and lower ribs.     

The histogenesis of rat intercostal muscle

Intercostal muscle from fetal and newborn rats was examined with the electron microscope. At 16 days' gestation, the developing muscle was composed of primary generations of myotubes, many of which were clustered together in groups. Within these groups, the membranes of neighboring myotubes were interconnected by specialized junctions, including tight junctions. Morphologically undifferentiated cells surrounded the muscle groups, frequently extended pseudopodia along the interspace between adjacent myotubes, and appeared to separate neighboring myotubes from one another. At 18 and 20 days' gestation, the muscle was also composed of groups of cells but the structure of the groups differed from that of the groups observed at 16 days. Single, well differentiated myotubes containing much central glycogen and peripheral myofibrils dominated each group. These large cells were interpreted as primary myotubes. Small, less differentiated muscle cells and undifferentiated cells clustered around their walls. Each cluster was ensheated by a basal lamina. The small cells were interpreted as primordia of new generations of muscle cells which differentiated by appositional growth along the walls of the large primary myotubes. All generations of rat intercostal muscle cells matured to myofibers between 20 days' gestation and birth. Coincidentally, large and small myofibers diverged from each other, leading to disintegration of the groups of muscle cells. Undifferentiated cells frequently occurred in the interspaces between neighboring muscle cells at the time of separation. Myofibers arising at different stages of muscle histogenesis intermingled in a checkerboard fashion as a result of this asynchronous mode of development. The possibility of fusion between neighboring muscle cells in this developing system is discussed.     

Phrenic and external intercostal motoneuron activity during progressive asphyxia

Phrenic and external intercostal motoneuron activities were compared during progressive asphyxia induced by the interruption of artificial ventilation in the pentobarbital-urethan-anesthetized, gallamine-paralysed rabbit. The relative augmentation of inspiratory activity of the T1-T4 external intercostal nerves was significantly greater than that of the phrenic nerve during asphyxic hyperpnea. This was associated with a greater recruitment of intercostal than of phrenic motoneurons, particularly late in the hyperpneic phase immediately before the period of asphyxic apnea. However, peak and average discharge frequencies developed by intercostal motoneurons (n = 20) were only approximately 60% of those of the phrenic motoneurons (n = 28). Gasping respiration terminated the apneic period and was associated with a further intense recruitment of intercostal though not of phrenic motoneurons, but discharge frequencies developed by the intercostal motoneurons remained approximately 60% of those of the phrenic motoneurons. The instantaneous frequency profiles generated by the motoneurons often exhibited progressive changes during the terminal stages of hyperpnea (reduction in inspiratory duration and duty cycle and increases in inspiratory slope and discharge frequencies) such that much of the character of gasping respiration became evident before the apnea. Such smooth transitional sequences do not obviate the existence of an "independent gasping center" but do require that such a proposed center at least possess the capacity for interaction with those sites responsible for the generation of eupneic and hyperpneic respiration.