A. De Troyer

Mechanics of intercostal space and actions of external and internal intercostal muscles.

It is conventionally considered that because of their fiber orientations, the external intercostal muscles elevate the ribs, whereas the internal interosseous intercostals lower the ribs. The mechanical action of the intercostal muscles, however, has never been studied directly, and the electromyographic observations supporting this conventional thinking must be interpreted with caution. In the present studies, the external and internal interosseous intercostal muscles have been separately stimulated in different interspaces at, above, and below end-expiratory rib cage volume in anesthetized dogs. The axial (cephalo-caudal) displacements of the ribs were measured using linear displacement transducers. The results indicate that when contracting in a single interspace and other muscles are relaxed, both the external and internal intercostals have a net rib elevating action at end-expiratory rib cage volume. This action increases as rib cage volume decreases, but it progressively decreases as rib cage volume increases such that at high rib cage volumes, both the external and internal intercostals lower the ribs. Stimulating the intercostal muscles in three adjacent intercostal spaces simultaneously produced similar directional rib motion results. We conclude that (a) in contrast with the conventional thinking, the external and internal interosseous intercostals acting alone have by and large a similar effect on the ribs into which they insert; (b) this effect is very much dependent on rib cage (lung) volume; and (c) intercostal muscle action is primarily determined by the resistance of the upper ribs to caudad displacement relative to the resistance of the lower ribs to cephalad displacement. The lateral intercostals, however, might be more involved in postural movements than in respiration. Their primary involvement in rotations of the trunk might account for the presence of two differently oriented muscle layers between the ribs.

Rostrocaudal gradient of electrical activation in the parasternal intercostal muscles of the dog

1. Because the inspiratory mechanical advantage of the canine parasternal intercostal muscles is greatest in the third interspace and decreases gradually in the caudal direction, the electromyograms of these muscles in interspaces 3, 5 and 7 have been recorded in anaesthetized, spontaneously breathing dogs. Each activity was expressed as a percentage of the activity measured during tetanic, supramaximal stimulation of the internal intercostal nerve (maximal activity). 2. Parasternal inspiratory activity during resting, room air breathing was invariably greater in the third than in the fifth interspace (62.0 +/‐ 6.0 vs. 41.3 +/‐ 4.6% of maximal activity; P < 0.001) and smallest in the seventh interspace (22.8 +/‐ 2.7% of maximal activity; P < 0.001). This distribution of activity persisted during hyperoxic hypercapnia and during breathing against increased inspiratory airflow resistance. 3. This rostrocaudal distribution of activity also persisted after complete paralysis of the diaphragm as well as after deafferentation of the ribcage. 4. Studies of the distribution of the muscle fibre types indicated that the parasternal intercostals in all interspaces had a higher proportion of slow‐twitch oxidative (SO; type I) fibres than fast‐twitch oxidative‐glycolytic (FOG; type II a) fibres. 5. Thus the topographic distribution of parasternal inspiratory activity along the rostrocaudal axis of the ribcage is precisely matched with the topographic distribution of mechanical advantage. This extraordinarily effective pattern of activation probably results from the unequal distribution of central inputs throughout the parasternal motoneurone pool.

Rostrocaudal gradient of mechanical advantage in the parasternal intercostal muscles of the dog.

1. Previous theoretical studies have led to the predictions that, in the dog, the parasternal intercostal muscles in the rostral interspaces shorten more during passive inflation than those in the caudal interspaces and have, therefore, a greater inspiratory mechanical advantage. The present studies were undertaken to test these predictions. 2. The effects of passive inflation on the length of the parasternal intercostals interspaces 1 to 7 were evaluated with markers implanted in the costal cartilages. Although the muscles in all interspaces shortened with passive inflation, the fractional shortening increased from the first to the second and third interspaces and then decreased continuously to the seventh interspace. 3. To understand this peculiar distribution, a geometric model of the parasternal area was then developed and a relation was obtained between muscle shortening and the angles that describe the orientation of the muscle and costal cartilage relative to the sternum. Measurement of these angles indicated that the rostrocaudal gradient of parasternal shortening resulted from the different orientations of the costal cartilages and their different rotations during passive inflation. 4. The changes in airway pressure generated by the parasternal intercostals in interspaces 3, 5 and 7 were finally measured during selective, maximal stimulation. The fall in pressure was invariably greatest during contraction of the third interspace and smallest during contraction of the seventh. 5. These observations indicate that, in the dog, the rostrocaudal gradient in rib rotation induces a rostrocaudal gradient of mechanical advantage in the parasternal intercostals, which has its climax in the second and third interspaces. These observations also support the concept that the respiratory effect of a given respiratory muscle can be computed from its behaviour during passive inflation.

Differential control of the inspiratory intercostal muscles during airway occlusion in the dog.

1. The effect of airway occlusion on the electrical activity of the three groups of inspiratory intercostal muscles (external intercostal, levator costae, parasternal intercostal) situated in the cranial portion of the rib‐cage has been studied in thirty anaesthetized, spontaneously breathing dogs. 2. The three muscles were active during normal inspiration, and their activity was prolonged similarly during airway occlusion. However, a comparison of activity during occluded and unoccluded inspirations indicated that airway occlusion caused a facilitation of external intercostal and levator costae activities but an inhibition of parasternal intercostal activity. 3. The facilitation of external intercostal and levator costae activities was markedly reduced after section of the phrenic nerves and completely suppressed after section of the appropriate thoracic dorsal roots. 4. The inhibition of parasternal intercostal activity was not affected by section of the phrenic nerves or by section of the thoracic dorsal roots. This phenomenon, however, was abolished after bilateral cervical vagotomy. 5. Activation of the external intercostals and levator costae during inspiratory efforts are thus highly dependent on segmental reflexes arising in these muscles. In contrast, activation of the parasternal intercostals resembles that of the diaphragm in the sense that it depends primarily on the central respiratory drive.

The electro‐mechanical response of canine inspiratory intercostal muscles to increased resistance: the caudal rib‐cage.

1. The effect of graded increases in inspiratory airflow resistance and airway occlusion on the electrical activity and the mechanical behaviour of the levator costae and external intercostal muscles situated in the caudal interspaces (zone of apposition of the diaphragm to the rib‐cage) has been studied in spontaneously breathing dogs. 2. The external intercostal and levator costae muscles in the cranial interspaces were invariably active during unloaded inspiration and showed progressive facilitation of activity with increases in inspiratory resistance. In contrast, whether in the supine or in the prone position, the levator costae muscles of the caudal interspaces did not show any facilitation of activity, and the caudal external intercostal muscles never showed any inspiratory electrical activity, including during airway occlusion. 3. With graded increases in inspiratory airflow resistance, the cranial external intercostals demonstrated a gradual inspiratory lengthening and the cranial ribs were progressively displaced in the caudal direction. The caudal ribs, however, were invariably displaced in the cranial direction. As a result, the caudal external intercostals showed a progressive inspiratory shortening. 4. Shortening of the caudal external intercostals and cranial displacement of the caudal ribs were reproduced by isolated stimulation of the phrenic nerves. Thus, as inspiratory resistance increases, contraction of the diaphragm causes unloading, rather than loading, of the spindles present in the caudal external intercostal muscles. 5. After the phrenic nerves were sectioned, however, the caudal external intercostals invariably lengthened a substantial amount during inspiration, but they still did not show any inspiratory electrical activity. Accentuating the inspiratory lengthening of these muscles by external rib fixation and increasing the chemical respiratory drive did not elicit any inspiratory electrical activity either. The alpha‐motoneurones of the external intercostal muscles in the caudal interspaces thus have very small central respiratory drive potentials with respect to their critical firing threshold.

On the Intercostal Muscle Compensation for Diaphragmatic Paralysis in the Dog

1. Paralysis of the diaphragm in the dog is known to cause a compensatory increase in activation of the inspiratory intercostal muscles (parasternal intercostals, external intercostals, and levator costae). The present studies were designed to assess the mechanism(s) of that compensation. 2. Complete, selective diaphragmatic paralysis was induced by injecting local anaesthetic into small silicone cuffs placed around the phrenic nerve roots in the neck. 3. Paralysis produced a decrease in tidal volume and an increase in arterial P(CO2) (P(a,CO2)). The increased hypercapnic drive was a primary determinant of the increased inspiratory intercostal activity. 4. However, paralysis also produced an increased inspiratory cranial displacement of the ribs. When this increased rib displacement was reduced to that seen before paralysis, it appeared that the increase in external intercostal and levator costae inspiratory activity was commonly greater than anticipated on the basis of the increased P(a,CO2). 5. Diaphragmatic paralysis after bilateral vagotomy also elicited disproportionate increases in inspiratory intercostal activity, thus indicating that these increases are not caused by vagal afferent inputs. 6. These observations are consistent with the idea that the intercostal muscle compensation for diaphragmatic paralysis is, in part, due to the release of an inhibition originating from the contracting diaphragm. This inhibition might arise in the diaphragmatic tendon organs.

Rib motion modulates inspiratory intercostal activity in dogs.

1. A test was performed of the hypothesis that the motion of the ribs during inspiration modulates, via changes in spindle afferent activity, the activation of the inspiratory intercostal muscles. The electrical activity of the parasternal intercostal, external intercostal, and levator costae muscles in anaesthetized spontaneously breathing dogs was thus recorded during manipulation of the inspiratory displacement of the ribs over a wide range of rib motion. 2. In agreement with the hypothesis, the external intercostal and levator costae muscles lengthened and showed increased inspiratory activities when the normal inspiratory cranial motion of the lower rib was reduced or reversed into an inspiratory caudal motion. Conversely, the inspiratory activities decreased when the inspiratory cranial motion of the rib and the inspiratory shortening of the muscles was augmented. The inspiratory activity of the parasternal intercostal remained unchanged throughout. 3. However, when the two ribs making up the interspace were linked together so that the external intercostal muscle was constant in length, the relationship of muscle activity to rib motion was maintained. 4. In addition, when the upper rather than the lower rib of the interspace was manipulated, the relationship between the change in muscle length and inspiratory activity was reversed, so that activity decreased when the muscle was lengthened and increased when the muscle was shortened. The relationship of muscle activity to lower rib motion, however, was still maintained. 5. These observations thus indicate that rib motion triggers proprioceptive reflexes which, regardless of the changes in length of the individual muscles, make the external intercostal inspiratory activity exquisitely sensitive to the direction of rib displacement.

Intercostal muscle compensation for parasternal paralysis in the dog: central and proprioceptive mechanisms.

1. Denervation of the parasternal intercostal muscles in the dog is known to cause a substantial reduction in the inspiratory cranial displacement of the ribs and a compensatory increase in the activation of the other inspiratory intercostal muscles, namely the external intercostals and the levator costae. The present studies were designed to assess the mechanism(s) of that compensation. 2. Denervating the parasternal intercostals bilaterally caused a reduction in tidal volume and an increase in arterial PCO2 (Pa, CO2). Severing the parasternal intercostals selectively produced similar changes. The concomitant increases in external intercostal and levator costae activity, however, were much greater than predicted on the basis of the increased Pa, CO2. 3. Denervating the parasternal intercostals on one side of the chest produced large increases in ipsilateral, but not contralateral external intercostal activity. 4. Manipulating the ribs after the parasternal intercostals were inactivated so as to reproduce the normal inspiratory cranial displacement of the ribs elicited immediate, clear‐cut reductions in external intercostal and levator costae activities. 5. The increases in external intercostal and levator costae activities that occur after inactivation of the parasternal intercostals thus result partly from the increased hypercapnic drive but mostly from proprioceptive reflexes, presumably muscle spindle reflexes.

Effects of Paralysis with Pancuronium on Chest Wall Statics in Awake Humans

The influence of tonic inspiratory muscle activity on the relaxation characteristics of the chest wall, rib cage (RC), and abdominal wall (ABW) has been investigated in four highly trained subjects. Chest wall shape and volume were estimated with magnetometers. Pleural pressure (Pes) and abdominal pressure were measured with esophageal and gastric balloons, respectively. Subjects were seated reclining 30 degrees from upright, and respiratory muscle weakness was produced by pancuronium bromide until RC inspiratory capacity was decreased to 60% of control. Only minor changes were observed for Konno-Mead relaxation characteristics (RC vs. ABW) between control and paralysis. Similarly, although RC relaxation curves (RC vs. Pes) during paralysis were significantly different from control (P less than 0.05), the changes were small and not consistent. The differences between paralysis-induced changes in resting end-expiratory position of the chest wall and helium-dilution functional residual capacity (FRC) suggested changes in volume of blood within the chest wall. We conclude that 1) although tonic inspiratory activity of chest wall muscles exists, it does not significantly affect the chest wall relaxation characteristics in trained subjects; 2) submaximal paralysis produced by pancuronium bromide is likely to modify either spinal attitude or the distribution of blood between extremities and the thorax; these effects may account for the changes in FRC in other studies.