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Laboratory of Cardiorespiratory Physiology, Brussels School of Medicine and Chest Service, Erasme University Hospital, Brussels, Belgium; Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, Queen Square, London, United Kingdom; and Department of Aerospace Engineering and Mechanics, University of Minnesota, Minneapolis, Minnesota
ABSTRACT I. INTRODUCTION A. Anatomy of Intercostal Muscles B. Kinematics of the Ribs C. Historical Perspective II. RESPIRATORY EFFECTS OF INTERCOSTAL MUSCLES A. The Maxwell Reciprocity Theorem and Its Application to the Respiratory System B. Respiratory Effects of Intercostal Muscles in the Dog 1. Mechanical advantage 2. Muscle mass 3. Respiratory effect C. Mechanisms of the Respiratory Effects in the Dog D. Respiratory Effects of Intercostal Muscles in Humans 1. Mechanical advantage 2. Muscle mass 3. Respiratory effect E. Mechanisms of the Respiratory Effects in Humans F. Implication III. DISTRIBUTION OF NEURAL DRIVE TO THE INTERCOSTAL MUSCLES DURING BREATHING A. Distribution of Neural Drive in Quadrupeds B. Distribution of Neural Drive in Humans C. Implications IV. MECHANISMS FOR THE DISTRIBUTIONS OF NEURAL DRIVE TO THE INTERCOSTAL MUSCLES A. Intercostal Motor Units B. Peripheral Inputs to Intercostal Motoneurons C. Central Inputs to Intercostal Motoneurons D. Inhibitory and Modulatory Mechanisms V. MECHANICAL INTERACTIONS AMONG THE INSPIRATORY INTERCOSTAL MUSCLES A. Interactive Effects on Rib Cage Displacement B. Interactive Effects on the Lung C. Relative Contributions of the External and Parasternal Intercostals to Breathing VI. MECHANICAL INTERACTIONS BETWEEN THE INTERCOSTAL AND OTHER RESPIRATORY MUSCLES A. Interaction Between the Inspiratory Intercostals and the Neck Muscles B. Interaction Between the Inspiratory Intercostals and the Diaphragm C. Interaction Between the Expiratory Intercostals and the Abdominal Muscles VII. INFLUENCE OF LUNG VOLUME ON INTERCOSTAL MUSCLE ACTION VIII. WHY IS NEURAL DRIVE TO THE INTERCOSTAL MUSCLES MATCHED WITH MECHANICAL ADVANTAGE? A. The Mechanical System B. Minimum Work C. Minimum Metabolic Cost IX. SUMMARY AND CONCLUSIONS ACKNOWLEDGMENTS REFERENCES
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I. INTRODUCTION |
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A. Anatomy of Intercostal Muscles
The intercostal muscles form two thin layers that span each of the intercostal spaces. The outer layer, the external intercostals, extends from the tubercles of the ribs dorsally to the costochondral junctions ventrally. The fibers of this layer are oriented obliquely, in the caudal-ventral direction, from the rib above to the rib below. In contrast, the inner layer, the internal intercostals, extends from the sternocostal junctions to near the tubercles of the ribs, and its fibers run in the caudal-dorsal direction from the rib above to the rib below. Thus the intercostal spaces contain two layers of intercostal muscle in their lateral portion but a single layer in their ventral and sometimes in their dorsal portions. Dorsally, in the immediate vicinity of the vertebrae, there may be a small space without internal intercostal muscle fibers. The external intercostal muscle in this area, however, is duplicated in each interspace by the levator costae, a thin, triangular-shaped muscle that originates from the tip of the transverse process of the vertebra and fans out laterally to insert onto the caudal rib. Ventrally, between the sternum and the chondrocostal junctions, the external intercostals are replaced by a fibrous aponeurosis, the anterior intercostal membrane, and the only muscle fibers are those of the internal intercostals. This portion of the internal intercostals is distinguished from the interosseous portion by both its location and its function (see below) and is conventionally called the "parasternal intercostals."
Although the external intercostal muscle does not extend to the ventral region of the rib cage, the parasternal intercostals are covered on their inner surface by a thin muscle called the triangularis sterni or transversus thoracis. This muscle is not usually considered among the intercostal muscles, yet its fibers run cranially and laterally from the dorsal aspect of the caudal half of the sternum to the inner surface of the costal cartilages of the third to seventh ribs. These fibers, therefore, are oriented nearly perpendicular to those of the parasternal intercostals and parallel to the external intercostals.
All the intercostal muscles in a given interspace are innervated by the corresponding intercostal nerve, and although there may be differences in detail among species, the general pattern of innervation is fairly constant. From its origin in the thoracic segment of the spinal cord, the intercostal nerve runs ventrally, between the pleura and the caudal aspect of the rib making up the rostral border of the interspace, and it sends many fine nerve branches (or filaments) (188) along its course to supply the entire internal intercostal muscle, including the parasternal intercostal, the triangularis sterni, and several abdominal muscles. The main nerve trunk, therefore, is commonly called the "internal intercostal nerve" (188). However, this nerve trunk also sends two large branches along its course. In the dorsal portion of the interspace, near the rib angle, the nerve sends a first large branch that perforates the internal intercostal muscle and then runs ventrally between the external and internal intercostal muscles. This large branch innervates, through a number of fine filaments, the external intercostal muscle and is usually referred to as the "external intercostal nerve" (188). The second large branch perforates both the internal and external intercostal muscles about halfway between the rib angle and the costochondral junction and innervates the external oblique muscle of the abdomen; this branch and the internal intercostal nerve also have cutaneous components.
The mechanical action of any skeletal muscle is essentially determined by the anatomy of the muscle and by the structures it displaces when it contracts. The intercostal muscles are morphologically and functionally skeletal muscles, and the primary effect of their contraction is to displace the ribs and thereby to alter the configuration of the rib cage. An understanding of the actions of the intercostal muscles, therefore, requires a clear understanding of the mechanics of the ribs and the rib cage.
Each rib articulates at its head with the bodies of its own vertebra and of the vertebra above, and at its tubercle with the transverse process of its own vertebra. The head of the rib is closely connected to the vertebral bodies by radiate and intra-articular ligaments, such that only slight gliding movements of the articular surfaces can occur. Also, the neck and tubercle of the rib are bound to the transverse process of the vertebra by short ligaments that limit the movements of the costotransverse joint to slight cranial and caudal gliding. As a result, the costovertebral and costotransverse joints together form a hinge, and the respiratory displacements of the rib occur primarily through a rotation around the long axis of its neck, as shown in Figure 1A (111, 112, 144, 210). This axis is oriented laterally, dorsally, and caudally. In addition, the ribs are curved and slope caudally and ventrally from their costotransverse articulations, such that their ventral ends and the costal cartilages are more caudal than their dorsal ends (Fig. 1, B and C). When the ribs are displaced in the cranial direction, therefore, their ventral ends move laterally and ventrally as well as cranially, the cartilages rotate cranially around the chondrosternal junctions, and the sternum is displaced ventrally. Consequently, both the lateral and dorsoventral diameters of the rib cage usually increase (Fig. 1, B and C). Conversely, a caudal displacement of the ribs is usually associated with a decrease in rib cage diameters. This implies that the muscles that elevate the ribs have an inspiratory effect on the rib cage, whereas the muscles that lower the ribs have an expiratory effect on the rib cage.
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The respiratory functions of the intercostal muscles have been controversial throughout medical history. The archival literature on the subject, in fact, extends back to Galen (
130–200 A.C.) who states that the "outer set effects breathing out, the inner breathing in" (83); in other words, the external intercostals have an expiratory action, and the internal intercostals have an inspiratory action. In the Renaissance period, however, Leonardo da Vinci (1452–1519) came to the opposite conclusion (160). Leonardo produced a number of drawings related to the anatomy and the physiology of the respiratory system, and one of them shows a lateral view of the thorax with the ribs and intercostal muscles exposed (Fig. 2, Ref. 112a). The text associated with this drawing states that the fibers interposed between the ribs along the obliquity of the internal intercostals serve to expel the inspired air and that the fibers on the outer side of the ribs in an obliquity contrary to the internal intercostals serve to dilate the ribs and open the lung to take in new air. These thoughts, however, remained largely unknown and had little influence on subsequent opinion. Indeed, Vesalius (1514–1564) stated a little later that both the external intercostals and the internal intercostals are expiratory muscles (202), whereas Borelli (1608–1679) maintained that both are inspiratory muscles (10).
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This theory is based on an analysis of the model of the ribs and intercostal muscles shown in Figure 3. When an intercostal muscle contracts in one interspace, it pulls the upper rib down and the lower rib up. However, because the fibers of the external intercostal slope caudad and ventrally from the rib above to the rib below, their lower insertion is further from the center of rotation of the ribs (i.e., the costovertebral articulations) than their upper insertion. Consequently, when these fibers contract, exerting equal and opposite forces at the two insertions, the torque acting on the lower rib, which tends to raise it, is greater than that acting on the upper rib, which tends to lower it. The net effect of the external intercostal, therefore, would be to raise the ribs and, with it, to inflate the lung. On the other hand, the fibers of the internal intercostal slope caudad and dorsally from the rib above to the rib below, such that their lower insertion is less distant from the center of rotation of the ribs than their upper insertion. As a result, the torque acting on the lower rib is smaller than that acting on the upper rib, so the net effect of the muscle would be to lower the ribs and to deflate the lung. Hamberger (94) also concluded that the action of the parasternal intercostals should be referred to the sternum, rather than the spine. Therefore, even though these muscles are part of the internal intercostal layer, their contraction should raise the ribs and inflate the lung.
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In the last 15 years, studies have been performed, first in dogs and then in humans, that have led to significant progress in the assessment and understanding of the respiratory actions of the intercostal muscles. This review summarizes these recent developments. One of the most intriguing aspects of these has been the observation of a remarkable relationship between the spatial distribution of neural drive to the intercostal muscles and the spatial distribution of mechanical advantage. This review, therefore, also discusses the possible mechanisms for the distribution of neural drive to the muscles and the possible teleological reasons for such a relationship. The review finally examines the mechanical interactions among the different sets of intercostal muscles and between these muscles and the other muscles involved in the act of breathing, in particular the diaphragm and the abdominal muscles. The nonrespiratory functions of the intercostal muscles, however, in particular their roles in posture maintenance (145), trunk rotation (176, 203), coughing, and vomiting (107, 129, 148, 157), are not covered.
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II. RESPIRATORY EFFECTS OF INTERCOSTAL MUSCLES |
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Many intercostal muscles are inaccessible and cannot be activated in isolation. The respiratory effects of these muscles, therefore, have been assessed in recent years by using an indirect method. This method is based on the reciprocity theorem of Maxwell (147). This standard theorem of mechanics applies to any linear elastic system and states that in such a system, the displacement of one point, per unit force applied at a second point, equals the displacement of the second point, per unit force applied to the first point. When applied to the chest wall, this theorem therefore states that the change in lung volume per unit force applied by a muscle is related to the change in length of the muscle when the relaxed chest wall is passively inflated by applying a pressure at the airway opening (206, 207). This relationship can be put in the following form where 
Pao denotes the change in airway opening pressure produced by muscle contraction with the airway occluded, m denotes muscle mass, 
denotes the active muscle tension per unit cross-sectional area, and L/L denotes the fractional change in muscle length per unit volume increase of the relaxed chest wall (VL)Rel
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For a machine, such as a lever, mechanical advantage is defined as the ratio of the force delivered at the load to the force applied at the handle. By analogy, the mechanical advantage of a respiratory muscle may therefore be defined as Pao/m and, according to Equation 1, could be evaluated by measuring [L/(LVL)]Rel. In other words, a muscle that shortens during passive inflation (negative L/L) would have an inspiratory mechanical advantage and would cause a fall in Pao when it contracts alone. Conversely, a muscle that lengthens during passive inflation (positive L/L) would have an expiratory mechanical advantage and would cause a rise in Pao during isolated contraction. Also, in this review, the respiratory effect of a muscle is defined as the value of Pao that is produced by the muscle during a maximal, isolated contraction at its optimal force-producing length (Lo).
The validity of Equation 1 as a predictor of respiratory effect was initially tested on the canine parasternal intercostal muscles (54). The animals were anesthetized, placed in the supine posture, and made apneic by mechanical hyperventilation, and the fractional changes in length of the muscle bundles situated near the sternum in the third, fifth, and seventh interspaces were measured during passive inflation of the respiratory system. Next, the internal intercostal nerves in the three interspaces were exposed at the chondrocostal junctions on both sides of the sternum, and with the animal still apneic, the endotracheal tube was occluded. Stimuli of supramaximal voltage were then delivered to the nerves, and the Pao generated by the sternal portion of each parasternal intercostal was measured. The muscle in each interspace was finally harvested, and its mass was measured.
The results of this experiment are shown in Figure 4. With passive inflation, the parasternal intercostal muscle bundles near the sternum shortened in all interspaces, but the fractional muscle shortening decreased from the third to the fifth interspace and decreased further to the seventh interspace. Also, during isolated stimulation, the muscles in all interspaces caused a fall in Pao, thus confirming that they have an inspiratory effect. Moreover, Pao/m was consistently greater for the third interspace than for the fifth, and the latter, in turn, was greater than Pao/m for the seventh interspace. Thus Pao/m for these muscles was proportional to the fractional change in muscle length during passive inflation. In addition, the slope of the relationship between Pao/m and the change in muscle length during passive inflation should be the maximal active muscle tension per unit cross-sectional area (), and in vitro measurements of this variable in a number of limb and respiratory muscles in animals and in humans have yielded values ranging between 2.2 and 3.5 kg/cm2 (19, 77, 78). As shown in Figure 4, a line with a slope of 3.0 fitted the data on the canine parasternal intercostals well.
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Pao/m. In contrast, the triangularis sterni in each interspace showed a large fractional lengthening during passive inflation, and its isolated stimulation caused a large Pao/m, in particular when the stimulation was performed after the length of the muscle was brought near Lo by passive inflation. As a result, Pao/m was uniquely related to [L/(LVL)]Rel for all the muscles, and the coefficient of proportionality () between the two was 3.0 kg/cm2.
The linearity assumption that underlies Maxwell's theorem was also tested by assessing the interactions between various inspiratory muscles on the lung. Indeed, in a linear elastic system, the resultant effect of different forces acting simultaneously is the sum of the effects of the individual forces. Therefore, if the chest wall were reasonably linear and elastic, the effects of active forces in several muscles on Pao should be additive. Legrand et al. (139) have stimulated electrically the parasternal intercostals and the interosseous (both external and internal) intercostal muscles in dogs with the endotracheal tube occluded, first in two interspaces separately and then in the same two interspaces simultaneously. The Pao measured during simultaneous stimulation of the muscles in two interspaces was, within 10%, equal to the sum of the Pao values produced by stimulation of the muscles in each individual interspace. The Pao produced by the simultaneous contraction of the parasternal intercostals in one interspace and either the scalenes or the sternomastoids was also found to be nearly equal to the sum of the Pao values produced by the two sets of muscles individually (139), and similar results were obtained for both the parasternal intercostals and the interosseous intercostals situated on the left and right sides of the sternum (16). Thus, in all these cases, the changes in intrathoracic pressure generated by the rib cage muscles were essentially additive, and this finding, combined with the results summarized in Figure 4, provides strong support for the idea that the reciprocity theorem of Maxwell is applicable to the respiratory system. Therefore, to assess the respiratory effects of the external and internal interosseous intercostals in dogs, De Troyer et al. (55) measured the masses of the muscles throughout the rib cage and their fractional changes in length during passive inflation, and for each muscle area, they multiplied L/L by m and by 3.0.
B. Respiratory Effects of Intercostal Muscles in the Dog
The fractional changes in length of the canine external intercostal muscles in the dorsal third, middle third, and ventral third of the even-numbered interspaces during passive inflation are shown in Figure 5A. With passive inflation, the muscle in the dorsal third of the second interspace shortened markedly; that is, this muscle area has a large inspiratory mechanical advantage. However, this inspiratory mechanical advantage decreases continuously toward the base of the rib cage, such that it is abolished in the 8th interspace and reversed into an expiratory mechanical advantage in the 10th interspace. In addition, the external intercostal in any given interspace has a smaller inspiratory mechanical advantage or a greater expiratory mechanical advantage as one moves from the angle of the ribs toward the costochondral junctions. As a result, the muscles in the ventral third of the sixth interspace and in the middle and ventral thirds of the 8th and 10th interspaces also have an expiratory mechanical advantage (55).
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The mechanical advantage of the levator costae has not been assessed. To the extent that the muscle fibers originate from the transverse process of the vertebra and insert on the caudal rib, however, it is clear that the muscle in every interspace has an inspiratory mechanical advantage. As for the external intercostal in the dorsal portion of the rib cage, this inspiratory mechanical advantage would also be expected to decrease gradually with increasing interspace number. In contrast, as pointed out in the previous section, the triangularis sterni has a large expiratory mechanical advantage in all interspaces (51).
In the dog, external intercostal muscle mass is greatest in the dorsal third of the rostral interspaces, and it decreases progressively both toward the base of the rib cage and toward the costochondral junctions (55). Conversely, although the mass of internal interosseous intercostal muscle does not demonstrate any clear-cut dorsoventral gradient, it shows a threefold increase from the rostral to the caudal interspaces. Thus the spatial distributions of external and internal intercostal muscle masses are essentially the same as the spatial distributions of mechanical advantage.
Both muscles, however, are thinner than the parasternal intercostals. In animals with body masses between 15 and 25 kg, the mass of parasternal intercostal muscle in a given interspace (both sides of the sternum) is 10–11 g. In contrast, the mass of external intercostal muscle in a given rostral interspace is only 4–5 g, and the mass of internal interosseous intercostal muscle ranges from 2.5 g in the most rostral interspaces to 7.5 g in the caudal interspaces. As a result, the total mass of parasternal intercostal in interspaces 1–8 is 75 g, whereas the total masses of external and internal interosseous intercostal in interspaces 1–10 are 45 and 54 g, respectively.
The respiratory effects computed as described above for the different areas of external and internal intercostal muscle in the dog are shown in Figure 6. These effects have essentially the same distributions as the mechanical advantages, but these are modified by the effect of mass distribution (55). Thus the external intercostals in the dorsal third of the rostral interspaces have an inspiratory effect, whereas those in the middle third and ventral third of the caudal interspaces have an expiratory effect (Fig. 6A). Also, the internal interosseous intercostals in the caudal interspaces have an expiratory effect, whereas those in the ventral third of the most rostral interspaces have an inspiratory effect (Fig. 6B). However, because the external intercostals in the dorsal third of the rostral interspaces and the internal interosseous intercostals in the caudal interspaces have larger masses, their respective inspiratory and expiratory effects are enhanced. Similarly, the mass of the sternal portion of the parasternal intercostal in a particular rostral interspace is greater than the mass of the external intercostal in the dorsal third of the same interspace by a factor of 2. Consequently, the former muscle areas have greater inspiratory effects than the latter (Fig. 6B).
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We have pointed out in the previous section that the Pao values generated by the canine parasternal or interosseous intercostals in adjacent interspaces are essentially additive. It is most likely, therefore, that the Pao generated by the areas of external or internal interosseous intercostal muscle in the dorsal third, the middle third, and the ventral third of a particular interspace are also additive, and Figure 7 shows the results of such additions for the different even-numbered interspaces; the respiratory effects of the sternal half of the parasternal intercostals are also shown for comparison. The external intercostal in the second interspace has a total inspiratory effect that is similar to the effect of the sternal portion of the parasternal intercostal in the same interspace. However, the inspiratory effect of the external intercostals decreases rapidly from the second to the sixth interspace, and it is reversed into an expiratory effect in the 8th and 10th interspaces. On the other hand, the internal interosseous intercostals in the 8th and 10th interspaces have a large expiratory effect, and although this effect decreases markedly in the cranial direction, it remains expiratory up to the fourth or third interspace. As a result, a maximal contraction of the internal interosseous intercostals in all interspaces would have a definite expiratory effect, whereas a maximal contraction of all the external intercostals would have little or no effect. In contrast, even though the inspiratory effect of the sternal half of the canine parasternal intercostals also decreases from the second interspace to the eighth (Figs. 6 and 7), a maximal contraction of these muscle bundles in all interspaces would have a clear-cut inspiratory effect.
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Pao values measured experimentally for the parasternal intercostals and the triangularis sterni are very close to the computed values. For the external and internal interosseous intercostals, however, the only data that can be compared with the computed Pao values are those reported by Ninane et al. (169), and these data differ slightly from the computed values. Thus these investigators produced electrical stimulation of the external and internal interosseous intercostals in the third and seventh interspaces in dogs by inserting pairs of copper wires between the two muscle layers from the costochondral junctions to the angles of the ribs; the two intercostal muscles, therefore, were activated simultaneously. When the muscles in the third interspace were activated, pleural pressure (Ppl) fell by 0.5–1.9 cmH2O, and these values agree reasonably well with the computed values. Indeed, if one assumes that the pressure changes produced by the external and internal intercostals in a given interspace are additive, the computed values for the second and fourth interspaces are –1.35 and –0.50 cmH2O, respectively. On the other hand, when Ninane et al. (169) stimulated the muscles in the seventh interspace, they recorded no change in Ppl, whereas the computed Pao values for the sixth and eighth interspaces indicate clear-cut expiratory effects.
This difference may be accounted for, at least in part, by the technique of stimulation used by these investigators (169); that is, because the stimulations were made through wires inserted from the costochondral junctions to the rib angles, they probably involved the levator costae muscle as well. As this muscle has an inspiratory effect, its activation should obscure or at least reduce the expiratory effect of the external and internal interosseous intercostals in the seventh interspace. More importantly, the Ppl values reported by Ninane et al. (169) were obtained during stimulation at resting end-expiration (functional residual capacity, FRC). On the other hand, the computed Pao values refer to the pressure changes that the muscles produce during maximal activation at Lo, and the studies of the canine triangularis sterni have clearly illustrated the critical importance of muscle length in determining the Pao generated by expiratory muscles (51). Specifically, when the triangularis sterni in a single interspace was bilaterally stimulated at 1.0 liter above FRC (the muscle then was placed in the vicinity of Lo), Pao averaged +1.75 cmH2O, but when the muscle was stimulated at FRC, Pao was only +0.80 cmH2O. In view of the substantial lengthening of the external and internal interosseous intercostals in the caudal interspaces during passive inflation (Fig. 5), it is most likely that the lung volume corresponding to the Lo of these muscles is also well above FRC. Consequently, their force-generating ability at FRC should be less than maximum. Ninane et al. (169) did not stimulate the muscles after maximal inflation, yet they reported that the Ppl produced by the external and internal interosseous intercostals in the seventh interspace increased from 0 to +0.4 cmH2O when lung volume was moderately increased above FRC by applying a transrespiratory pressure of +10 to 15 cmH2O. Irrespective of the probable coactivation of the levator costae, this result fully supports the idea that the intercostal muscles in the caudal interspaces, when activated at appropriate lung volumes, have an expiratory effect on the lung.
C. Mechanisms of the Respiratory Effects in the Dog
As we have pointed out in section IB, the theory of Hamberger (94) maintains that as a result of the orientation of the muscle fibers, the external intercostals and the parasternal intercostals have an inspiratory effect and that the internal interosseous intercostals have an expiratory effect. And indeed, in the dog, the external intercostals in the dorsal third of the rostral interspaces and the parasternal intercostals have inspiratory effects, whereas the internal interosseous intercostals over a large fraction of the rib cage have an expiratory effect (Fig. 6). However, the theory of Hamberger cannot explain the dorsoventral and rostrocaudal gradients of respiratory effect for the external and internal interosseous intercostals, and a multiple regression analysis of the data shown in Figure 6 indicates that the orientation of the muscle fibers accounts for only 20% of the total variance of the respiratory effect of these muscles; the position of the muscle fibers along the rib circumference accounts for another 10% of the variance, and interspace number accounts for 55%. In addition, in several areas of the rib cage, the sign of the respiratory effect of the muscles is opposite to that predicted by the theory, thus indicating that other mechanisms play a major role.
A major shortcoming of the theory of Hamberger is that it is based on a two-dimensional model of the rib cage; the ribs in the model are pictured as rigid straight rods and are assumed to rotate around axes that lie perpendicular to the plane of the ribs (Fig. 3). However, as Saumarez (185) and others (55, 208) have pointed out, real ribs are curved, and this curvature has critical effects on the moments exerted by the intercostal muscles, as shown in Figure 8A. The axis of rib rotation is oriented dorsally and laterally, and at point a on the rib, the tangent plane of the rib cage is perpendicular to the axis of rotation. For the external intercostal, therefore, the distance between the point of attachment of the muscle on the lower rib and the axis of rib rotation is greater than the distance between the point of attachment of the muscle on the upper rib and the axis of rotation. Consequently, at point a, the moment exerted by the muscle on the lower rib is greater than the moment exerted on the upper rib, and the net moment is inspiratory. However, at point b, the tangent plane of the rib cage lies parallel to the axis of rib rotation, so the distances between the points of attachment of the muscle on the two ribs and the axes of rib rotation are equal and the net moment exerted by the muscle is zero. Thus the net inspiratory moment of the external intercostal is maximum in the dorsal region of the rib cage, decreases to zero at point b, and is reversed to an expiratory moment in the ventral region of the rib cage (Fig. 8B). On this basis, the dorsoventral decrease in the inspiratory effect of the external intercostals and the difference between the inspiratory effect of the external intercostals in the dorsal region of the rostral interspaces and the expiratory effect of the triangularis sterni can be understood. Similarly, the net expiratory moment of the internal intercostals is maximum in the dorsal region, decreases in magnitude as one moves away from the spine, and becomes an inspiratory moment in the vicinity of the sternum (Fig. 8B). The difference between the expiratory effect of the internal interosseous intercostals in the dorsal region of the rib cage and the inspiratory effect of the parasternal intercostals was already inferred by Hamberger, yet it was not appreciated that the differences between the actions of the muscles in the dorsal and ventral regions are the result of gradual transitions, not abrupt changes of mechanism at the costochondral junctions.
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In these studies, external forces were applied in the cranial direction to individual rib pairs in supine, paralyzed animals with the endotracheal tube occluded at FRC. Cranial rib displacement and Pao were measured as the force was increased, and these measurements revealed two important aspects of the mechanics of the rib cage. First, for a given force, rib displacement increased progressively with increasing rib number. Second, the Pao produced by a given rib displacement increased from the 2nd to the 5th rib pair and then decreased markedly from the 5th to the 11th rib pair. As a result, the ratio of Pao to applied force also increased with rib number in the more rostral interspaces and decreased markedly in the caudal interspaces, as shown in Figure 9 (closed circles). Therefore, although the forces exerted by a particular intercostal muscle on the upper and lower ribs are equal in magnitude (and opposite in direction), these forces have different effects on the lung. Specifically, in the rostral half of the rib cage, the fall in Pao produced by the cranial force on a particular rib is larger than the rise in Pao caused by the caudal force on the rib above, so a hypothetical intercostal muscle lying parallel to the longitudinal body axis would have a net inspiratory action on the lung during isolated contraction. On the other hand, in the caudal half of the rib cage, the fall in Pao produced by the cranial force on a particular rib is much smaller than the rise in Pao produced by the caudal force on the rib above, so an intercostal muscle lying parallel to the longitudinal body axis would have a net expiratory effect. In other words, the nonuniform coupling between the ribs and the lung confers an inspiratory bias to both the external and internal interosseous intercostals in the rostral interspaces and an expiratory bias to both muscle groups in the caudal interspaces.
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The conclusion thus can be drawn that the respiratory effects of the canine intercostal muscles are the result of two mechanisms (208). The predominant mechanism is the nonuniform coupling between the ribs and the lung and the consequent difference between the respiratory effects of equal and opposite forces on adjacent ribs. This mechanism has a larger effect in the ventral region of the rib cage than in the dorsal region, and it causes the dependence of respiratory effect on interspace number. The second mechanism is the "Hamberger mechanism," modified to account for the three-dimensionality of the rib cage. This mechanism is the result of the difference between the magnitudes of the moments applied to the upper and lower ribs of an interspace, and this difference, in turn, depends on the orientation of the muscle. The magnitude of the effect of this mechanism is larger in the dorsal region of the rib cage than in the ventral region, and its sign is reversed in the vicinity of the costochondral junctions. It is responsible for the difference between the respiratory effects of the external and internal intercostals. Although these two mechanisms operating together account well for the respiratory effects of the external and internal intercostals in most interspaces, it must be stressed that they do not explain the large expiratory effects of the muscles in the most caudal interspaces. At this point, the mechanism for these large expiratory effects is still unclear.
D. Respiratory Effects of Intercostal Muscles in Humans
The intercostal muscles in humans are even less accessible than those in the dog. Their respiratory effects, therefore, were assessed by the following method. The muscles were first dissected in cadavers to measure the orientations of the muscle fibers relative to the ribs and to determine muscle masses (m in Eq. 1) (209). Although the cadavers were carefully selected and did not show any evidence of overt undernutrition, they had a 50% reduction in scalene and sternomastoid muscle mass compared with young healthy individuals (138). It was assumed, therefore, that the intercostal muscles in cadavers were similarly atrophied and, hence, the measured values of intercostal muscle mass were multiplied by two. Healthy individuals were then placed in a computed tomographic (CT) scanner to determine the shape of the ribs and their precise transformation during passive inflation, and from these data, the fractional changes in length of lines having the orientations of external and internal interosseous intercostals were computed so as to assess the mechanical advantages of the muscles {[L/(LVL)]Rel in Eq. 1}. The mechanical advantages of the parasternal intercostals and triangularis sterni were similarly computed from values of the orientation of the costal cartilages obtained from CT images (53). The values of mechanical advantage were finally multiplied by the values of muscle mass, measured in cadavers and corrected for muscle atrophy, and by (i.e., 3.0 kg/cm2) to evaluate the respiratory effects of the muscles throughout the rib cage (53, 209).
The topographic distribution of mechanical advantage among the external intercostal and parasternal intercostal muscles in humans is qualitatively similar to that in the dog. As in the dog, the human external intercostals in the dorsal portion of the rostral interspaces (and presumably the levator costae) have a clear-cut inspiratory mechanical advantage, and this inspiratory mechanical advantage decreases continuously toward the base of the rib cage and toward the costochondral junctions. As a result, the external intercostals in the ventral portion of interspaces 6–8 have an expiratory mechanical advantage. Also, the parasternal intercostal muscle in every interspace has an inspiratory mechanical advantage, and this advantage decreases gradually from the second to the fifth interspace. It must be pointed out, however, that in humans, the parasternal intercostals do not extend beyond the fifth interspace, and the mechanical advantage of the muscle in that interspace is very small.
As in the dog, the triangularis sterni muscle in humans has an expiratory mechanical advantage in every interspace, and this is particularly strong in the more caudal (5th and 6th) interspaces. The internal interosseous intercostals in humans also have an expiratory mechanical advantage throughout the rib cage. The striking difference observed in the dog between the interosseous and intercartilaginous portions of the internal intercostals is thus maintained in humans. However, the topographic distribution of the expiratory mechanical advantage of the internal interosseous intercostals in humans differs from the dog in two respects. First, the expiratory mechanical advantage of the muscle in the dorsal portion of the rib cage in humans decreases from the top to the base of the rib cage, whereas in the dog, it gradually increases. Second, the expiratory mechanical advantage of the muscle in humans is greatest in the ventral portion, rather than the dorsal portion of the caudal interspaces. These differences are probably the result of the species differences in rib cage shape and rib displacements (see sect. IIE).
The topographic distribution of external intercostal muscle mass in humans is also qualitatively similar to that observed in the dog. The mass of the muscle is thus greatest in the dorsal half of the rostral interspaces, and from there it decreases gradually in both the caudal and the ventral direction. Consequently, the masses of the external intercostals in the dorsal half and the ventral half of the eighth interspace are only 61 and 35%, respectively, of the muscle mass in the dorsal half of the second interspace. On the other hand, the mass of internal interosseous intercostal muscle in humans does not show any definite rostrocaudal gradient and is slightly larger in the ventral than in the dorsal portion of the rib cage.
The masses of external and internal interosseous intercostal muscle in humans, however, are much larger than the masses of parasternal intercostal and triangularis sterni muscle (53, 209). Thus, after the values of muscle mass measured in the cadavers were corrected for muscle atrophy, the average total mass of external intercostal muscle in interspaces 1–8 was 208 g, and the average total mass of internal interosseous intercostal was 138 g. In contrast, the total masses of the parasternal intercostals and triangularis sterni were only 32 and 18 g, respectively.
The maximum Pao values computed for the areas of external and internal intercostal muscle in the dorsal half and the ventral half of the different even-numbered interspaces in humans are shown in Figure 10. As a result of the distributions of mechanical advantage and muscle mass, the effect of the external intercostals in the dorsal portion of the rostral interspaces is clearly inspiratory (Fig. 10A). As in the dog, however, this effect shows definite dorsoventral and rostrocaudal gradients, such that the Pao values for the muscles in the dorsal half of the fourth interspace and the ventral half of the second interspace are only half the value for the muscle in the dorsal half of the second interspace. The computed Pao values for the external intercostals in the dorsal half of the sixth and eighth interspaces are even lower, and in the ventral half of these caudal interspaces, the respiratory effect of the external intercostal is reversed into an expiratory effect. Although the internal interosseous intercostals in humans have an expiratory effect throughout the rib cage, they also demonstrate strong dorsoventral and rostrocaudal gradients (Fig. 10B).
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Pao values generated by the areas of external or internal interosseous intercostal muscle in the dorsal and ventral portions of a particular interspace in humans are additive, the total inspiratory effect of the external intercostal in the second interspace is therefore approximately five times greater than the inspiratory effect of the parasternal intercostal in the same interspace (Fig. 11). Such a difference is also present in the fourth and sixth interspaces, although the inspiratory effects of both muscles in these interspaces are smaller. In contrast, the internal interosseous intercostals have a definite expiratory effect in all interspaces, even though this effect decreases gradually from the eighth to the second interspace (Fig. 11). Because the mass of the internal intercostal muscle in a given interspace is much greater than the mass of the triangularis sterni, the total Pao value computed for the internal intercostal in the sixth interspace, for example, is approximately seven times greater than the computed Pao value for the triangularis sterni in the same interspace.
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We have emphasized in section IIC that the respiratory effects of the intercostal muscles in the dog are the result of two mechanisms. The first mechanism is the nonuniform coupling between the ribs and the lung and the consequent difference between the respiratory effects of equal and opposite forces on adjacent ribs. This mechanism has a greater effect in the ventral region of the rib cage than in the dorsal region, and as in the dog, the human intercostals in the ventral region do have an inspiratory bias in the second interspace and an expiratory bias that increases with interspace number in the more caudal interspaces (Fig. 10). Thus, although it has not been possible, as yet, to assess the coupling between the ribs and the lung in humans, the observed distributions of the respiratory effects of the human intercostal muscles suggest that this coupling has a similar pattern to that in the dog. The second mechanism, the "Hamberger mechanism," is the result of the orientation of the muscle fibers and the difference between the moments exerted by these fibers on adjacent ribs. The external and internal intercostal muscles have similar orientations in humans and in the dog. In humans, however, the rib cage at FRC is larger along its lateral than its dorsoventral axis, whereas in the dog, as in most quadrupeds, it is larger along its dorsoventral axis. Consequently, the tangent plane of the rib cage in the dorsal region is close to perpendicular to the axis of rib rotation over a longer portion of the rib circumference in humans than in the dog, so the large inspiratory moment of the external intercostals in the dorsal region and the large expiratory moment of the internal intercostals should be better maintained. In addition, the ribs in humans are slanted caudally more than those in the dog (144, 209). Therefore, the angle between the line of the internal intercostal muscle bundles and the longitudinal body axis is greater, and the difference between the distances from the points of attachment on the lower and upper ribs and the axes of rib rotation is also greater. As a result, the net moment is greater, and this should enhance the expiratory effect of the internal interosseous intercostals in the ventral portion of the caudal interspaces.
In the dog, both the external intercostal muscles and the internal interosseous intercostal muscles have an inspiratory effect in some areas and an expiratory effect in other areas (see sect. IIB). This implies that the function of these muscles during breathing depends on the topographic distribution of neural drive. For example, if the external intercostals in the dorsal region of the rostral interspaces were active during the inspiratory phase of the breathing cycle, they would inflate the lung. However, if the external intercostals in the ventral region of the caudal interspaces were active during the expiratory phase of the cycle, they would deflate the lung. Similarly, activation of the internal interosseous intercostals in the caudal interspaces during expiration would deflate the lung, but activation of the internal intercostals in the ventral region of the most rostral interspaces during inspiration would contribute to lung inflation. The results described in section IID similarly imply that in humans, the external intercostals could have an inspiratory function, an expiratory function, or both, depending on the spatial distribution of neural drive during inspiration and expiration.
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III. DISTRIBUTION OF NEURAL DRIVE TO THE INTERCOSTAL MUSCLES DURING BREATHING |
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Since the initial studies of Bronk and Ferguson (12), a number of electrical recordings from intercostal muscles and nerves in anesthetized cats (5, 92, 100, 124, 127, 188), dogs (32, 41, 46), and baboons (44) have shown that the parasternal intercostals, the external intercostals, and the levator costae are active during inspiration. On the other hand, the triangularis sterni and the internal interosseous intercostals are active during expiration (56, 73, 92, 106, 188, 194). In fact, it has been universally recognized that the parasternal intercostals and the levator costae are active only during inspiration and that the triangularis sterni is active only during expiration. In view of the mechanical advantage of the muscles (Figs. 4 and 5), the conclusion can therefore be drawn that in quadrupeds, the parasternal intercostals and levator costae have an inspiratory function during breathing, and the triangularis sterni has an expiratory function.
However, disparate reports of the activity patterns of the external and internal interosseous intercostals exist in the literature. Earlier studies in dogs by Gesell (87) also reported efferent discharges to the external intercostal muscles in the caudal interspaces during expiration and to the internal interosseous intercostal muscles in the most rostral interspaces during inspiration. Similar observations were made in decerebrate cats by LeBars and Duron (133) and in awake dogs by Carrier (18). Because the canine external intercostals in the caudal interspaces have an expiratory mechanical advantage and the internal interosseous intercostals in the most rostral interspaces have an inspiratory mechanical advantage (Fig. 5), these observations therefore raise the possibility that in the rostral interspaces, both the external and internal interosseous intercostals have inspiratory functions during breathing and that in the caudal interspaces, both have exp
) around the rib, as shown in B. The external intercostal muscle (continuous line) has the greatest inspiratory moment in the dorsal portion of the rib cage (
), 
) and 20 cmH2O (
) transrespiratory pressure; in contrast, for ribs 9 and 10, 
