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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.

Animals

[The structure of muscle spindles in the intercostal muscles and rectus abdominis of the human fetus].

The structure and innervation of muscle fibres were studied in external intercostal muscles and the streight muscle of the abdomen in 24--26-week human fetuses. The diameter of most spindles was shown to be within the range of 50--70 mkm, while in the streight muscle of the abdomen it could reach 100 mkm. In the external intercostal muscles the spindles, as a rule, were longer (300-500 mkm) than in the streight muscle of the abdomen (100--300 mkm) which was likely due to special functioning of the spindles in rhythmically working muscles. According to sensory innervation all the spindles may be divided into 3 main types: simple, intermediate and complex. In the external intercostal muscles there occur 3 types of spindles, while in the streight muscle of the abdomen there are spindles of a complex type.

Humans

Distribution of muscle fiber types and EMG activity in cat intercostal muscles.

The electromyogram (EMG) activity and histochemical properties of intercostal muscles in the anesthetized cat were studied. The parasternal muscles were consistently active during inspiration. The external intercostals in the rostral spaces and the ventral portions of the midthoracic spaces were also recruited during inspiration. The remaining external intercostals were typically silent, regardless of the level of respiratory drive. The internal intercostal muscles located in the caudal spaces were occasionally recruited during expiration. There was a clear correlation between recruitment patterns of the intercostals and the histochemically defined fiber type properties of the muscles. Intercostal muscles that were routinely recruited during inspiration had a significantly higher proportion of slow-oxidative muscle fibers.

Animals

Reflex and cerebellar influences on alpha and on 'rhythmic' and 'tonic' gamma activity in the intercostal muscle.

1. Efferent intercostal alpha and gamma activity and afferent intercostal muscle spindle activity were studied in decerebrate cats in response to stimulation of the anterior lobe of the cerebellum and to postural and other reflexes.2. Low threshold intercostal responses were elicited from lobuli IV and V of the anterior lobe of the cerebellum.3. The existence of two functionally different types of intercostal gamma neurones has been confirmed. These are the ;rhythmic' or ;specifically respiratory' gamma neurones, and the ;tonic' gamma neurones.4. In response to cerebellar stimulation, facilitatory, inhibitory and diphasic tetanic and post-tetanic effects were obtained from alpha and the two types of gamma fibres in both external and internal intercostal nerve branches.5. Generally both inspiratory and expiratory alpha and gamma activity was facilitated in response to tetanic stimulation at contralateral stimulus sites, and inhibited in response to stimulation of ipsilateral sites.6. ;Rhythmic' gamma activity appeared to be rather closely linked to the respiratory alpha activity but the balance between ;rhythmic' gamma and alpha was often changed in response to cerebellar stimulation, as indicated by the responses of primary muscle spindle afferents.7. The ;tonic' gamma neurones were as a rule more responsive to cerebellar stimulation than were the alpha and ;rhythmic' gamma neurones. Long-lasting post-tetanic effects were much more prominent in the ;tonic' gamma fibres than in the alpha or ;rhythmic' gamma fibres.8. ;Rhythmic' gamma activity was abolished after cervical transections of the cord. ;Tonic' gamma activity remained in the spinal preparations although usually at a different discharge rate.9. ;Tonic' gamma neurones were more responsive than the ;rhythmic' gamma neurones to the proprioceptive gamma reflex elicited by passive movements of the chest wall as well as to other spinal and supraspinal reflexes.10. Both ;dynamic' and ;static' gamma fibres seem to be represented in the group of ;tonic' intercostal gamma neurones.11. The significance of the results are discussed with regard to the following two main points: (a) integration of respiratory and postural functions of the intercostal muscles; (b) cerebellar control of the alpha-gamma balance in active contractions and passive relaxations.

Animals

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.

Adult

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.

Animals

Respiratory effects of stimulation of intercostal muscles and saphenous nerve in kittens.

Effects of intercostal muscle stimulation were studied in 2- to 7-day-old kittens under ketamine-acepromazine anesthesia. Animals were vagotomized, paralyzed, and artificially ventilated. Stimuli applied during inspiration (TI) inhibited this phase. Stimulus strength necessary for TI inhibition decreased with time. However, an all-or-nothing effect was not always observed. Stimulation during expiration (TE) prolonged this phase. The responsiveness increased with increasing stimulus delay. The effects of intercostal muscle stimulation were compared with those recorded during saphenous nerve stimulation. Stimulation during TI prolonged this phase. Phrenic activity increased after a short-lasting decrease in the on-going activity. Stimulation during the first 50% of TE had variable effects, whereas stimulation with longer delay shortened this phase. Our results indicated that the pattern of breathing in newborns can be affected by both intercostal muscle and other somatic efferents. However, the mechanisms controlling respiratory timing may differ in newborns and in adults. Different effects of respiratory muscle and saphenous nerve stimulation suggest different transmitters involved or different sites of interaction of these inputs with the medullary respiratory rhythm generator.

Animals

Intercostal muscles are used during rotation of the thorax in humans.

To test the idea that the lateral intercostal muscles may be more suited to aid in rotational than respiratory movements of the thorax, we inserted bipolar fine-wire electrodes in external and internal intercostal muscles in the right midaxillary line in nine sitting subjects and examined the pattern of contraction of these muscles during voluntary axial rotations of the thorax (30-35 degrees), resting breathing, and CO2-induced hyperpnea. The right external intercostal muscles were strongly recruited in rotations to the left but were not active in rotations to the right. In contrast, the right internal intercostal muscles were active in rotations to the right but not in rotations to the left. Rotations completed in 1 or 2 s were associated with an early burst of electromyographic activity, followed by a low plateau that persisted while the rotation was held. Rotations made very gradually over 5-10 s were associated with gradually rising electromyographic activity. The amplitude of activity recorded during 30-35 degrees rotations was equivalent to that measured when minute ventilation was increased by CO2 to 50 l/min. We conclude that the lateral intercostal muscles have a major role in producing axial rotations of the thorax.

Adult

Accuracy of reinnervation of rat internal intercostal muscles by their own segmental nerves.

The positions of internal intercostal motoneurons within their motor pool were studied, following reinnervation of the intercostal muscles by their original nerves. Six to 9 weeks after proximal nerve section in 10-d-old and adult rats, 0.1 microliter injections of wheat germ agglutinin (WGA)-HRP were made in the distal part of the reinnervated internal intercostal muscle. The corresponding region of the contralateral control muscle was also injected. The positions of the retrogradely labeled motoneurons were mapped in 100 microns transverse sections of thoracic spinal cord that had been stained for HRP according to the method of Mesulam (1982). In normal rats, motoneurons innervating distal muscle fibers are found largely in the more dorsal part of the internal intercostal motoneuron pool (Hardman and Brown, 1985). In adult rats, regenerated motor axons did not show any selectivity; distal muscle fibers were innervated by motoneurons whose cell bodies were distributed throughout the internal intercostal pool. However, in rats operated on at 10 d of age, distal intercostal muscle fibers were reinnervated by motoneurons that were distributed mainly in the dorsal part of the motor pool. These results support the view that positional signals may be of importance in organizing the distribution of axon terminals within muscles during development.

Aging

The effect of acute hemiplegia on intercostal muscle activity.

We recorded the EMG of parasternal intercostal muscles in 25 patients with flaccid hemiplegia during quiet spontaneous breathing, voluntary hyperventilation, and CO2-induced hyperventilation. The respiratory drive was abnormal on the hemiplegic side and the function of the intercostal muscles was affected specifically during voluntary hyperventilation.

Acute Disease

Experimental use of intercostal muscle flaps for repair of induced cardiac defects.

Intercostal muscle flaps were successfully used to repair 3 cm defects of the ventricular myocardium in the mongrel dog. Early and late healing of all flaps was uncomplicated and there were no late complications related to aneurysmal formation or electrical abnormalities of the heart. The existing blood supply of the heart was unaffected. The intercostal muscle is suggested as an alternative muscle flap for use in myocardial wall reconstruction.

Animals

Length changes of intercostal muscles during respiration in the cat.

Sonomicrometry was used to measure the length changes of intercostal muscles throughout the rib cage of anesthetized cats. The motor unit discharge in the vicinity of the length measurement was monitored with bipolar electrodes. The external intercostal muscles in the rostral spaces and the parasternals actively shortened during inspiration. The external intercostals in the caudal spaces, which were inactive, either shortened or lengthened passively due to the forces imposed on the lower rib cage by the contraction of the diaphragm. The length changes of external intercostals of the mid-thoracic spaces, which were recruited during inspiration, were variable. The internal intercostals were usually inactive in our preparation and therefore their length excursions passively followed those of the external intercostals. The information regarding the length changes is correlated with that previously gathered for the role of muscle spindles in the intercostal muscles. It is suggested that gamma motoneurons are recruited to prevent the muscle spindles from being unloaded when the intercostal muscle shortens and to increase the sensitivity of the receptors during the phase of the respiratory cycle when the muscle is active.

Animals

Mechanical action of the interosseous intercostal muscles as a function of lung volume.

On the basis of local stimulation of individual muscles, it has been suggested that both the external (EI) and internal interosseous intercostal muscles have an inspiratory action at low lung volumes and an expiratory action at high lung volumes. In this study, we assessed the action of the interosseous intercostal muscles at different lung volumes in 19 anesthetized dogs by synchronously activating the intercostal muscles via ventral root stimulation (VRS). An electrode was positioned on the upper thoracic spinal cord according to previously described techniques. The cervical phrenic rootlets were sectioned bilaterally, the accessory muscles were sectioned from the rib cage, and the origins of the abdominal muscles were sectioned from the middle region of the rib cage. Changes in airway pressure (delta P) were monitored during the application of supramaximal stimuli after hyperventilation-induced apnea and during airway occlusion. Animals were passively inflated or deflated with a volume syringe. Precontractile airway pressure was used as an index of lung volume. External and parasternal intercostal muscle (PA) lengths were monitored by sonomicrometry in the third intercostal space. Thoracoabdominal motion was monitored by Respitrace bands. During VRS, both PA and EI shortened at all lung volumes. Mean delta P progressively decreased with increasing lung volume. At precontractile airway pressures of -10, 0, and +30 cm H2O, delta P were -25 +/- 1, -16 +/- 1, and -5 +/- 1 cm H2O, respectively. After section of the internal intercostal nerves lateral to the costochondral junctions from the first through the seventh intercostal spaces to eliminate PA action, EI shortened, whereas PA usually lengthened.(ABSTRACT TRUNCATED AT 250 WORDS)

Airway Resistance

Recruitment of intercostal muscle activity during hypercapnia in kittens.

Little is known about the respiratory behavior of the intercostal muscles within a neonatal and developmental context. We, therefore, examined intercostal muscle electromyographic (EMG) activity in kittens (1 month old, n = 8; 2 months old, n = 7) during eupnea and heightened respiratory drive induced by hypercapnia. The kittens were anesthetized with halothane (1.25-1.50%) at comparable minimum alveolar concentrations and were studied in the prone position during an acute exposure to hyperoxic hypercapnia (8% CO2, 50% O2, balance N2) for 7 min. We recorded EMG activities from bipolar electrodes embedded in the intercostal (dorsolateral thorax, 4th-5th interspace) (EMGic) and costal diaphragm (EMGdi) muscles. Peak moving time average EMG measurements served as our index of muscle activity. Phasic inspiratory EMGic activity was present during eupnea in all animals. EMGic and EMGdi increased significantly above baseline levels during hypercapnic exposure with the increase in EMGic (133 +/- 27%) being comparable to that observed in EMGdi (141 +/- 28%) (P = 0.40). No differences in EMGic (P = 0.64) or EMGdi (P = 0.88) recruitment were noted between age groups. These data indicate that hypercapnia augments intercostal muscle EMG activity in kittens and suggest that such activity parallels costal diaphragmatic EMG recruitment. We conclude that EMGic recruitment is a frequent respiratory phenomenon associated with hypercapnically stimulated diaphragmatic muscle activity in kittens. We speculate that intercostal muscle recruitment stabilizes the compliant chest wall of the newborn and helps sustain inspiratory force generation during stimulated breathing.

Animals

External intercostal muscle activity during acute hypoxia in the kitten.

The effects of acute hypoxia on the recruitment of external intercostal muscle activity were determined in 12 kittens, aged 14 to 36 days. The animals were anesthetized with 1.23 +/- 0.23% halothane and bipolar electrodes were placed in the costal and crural diaphragm and in dorsal external intercostal muscles. Acute hypoxia was induced by the animals breathing 13% oxygen; arterial gases were sampled during baseline conditions and at 1 and 5 min after induction of hypoxia. Peak-moving average (PA) and minute electromyogram (EMG) activity (PA x f) were recorded during baseline conditions and at 1 and 5 min after onset of acute hypoxia. At 1 min of acute hypoxia, PA and PA x f of the costal diaphragm, crural diaphragm, and external intercostal muscles were significantly increased above baseline values (P less than 0.01). After 5 min of acute hypoxia, PA of all three muscles remained elevated above baseline values (P less than 0.05) but PA x f returned toward baseline levels. Respiratory frequency remained unchanged during the hypoxic stimulus. These data document that the newborn is capable of increasing inspiratory external intercostal muscle EMG activity during acute hypoxia. We speculate that this phasic recruitment could be of physiologic benefit to the newborn by stabilizing the complaint chest wall and by increasing the contribution of rib cage expansion to tidal breathing.

Acute Disease

Intercostal muscle action inferred from finite-element analysis.

The external and internal intercostal muscles are important respiratory muscles in humans, but their mechanical actions have been controversial. We used finite-element analysis based on anatomic and mechanical measurements in dogs to assess the action of the intercostal and other rib cage muscles in a model of an isolated canine rib cage. When intercostal muscle forces of either the internal or the external layer were applied in a single interspace, they pulled the adjacent ribs together, consistent with published observations in dogs. However, when the forces were applied in all interspaces, the external layer caused an inspiratory motion and the internal layer caused an expiratory motion, consistent with conventional understanding of intercostal muscle actions. Parasternal intercostal, levator costae, and transversus thoracis (triangularis sterni) muscle actions were also simulated. These muscles caused expected movements of the ribs and sternum. We conclude that the actions of intercostal muscles depend on the spatial extent of their activation. Their actions in a single interspace and in multiple interspaces can be observed and explained with three-dimensional finite-element models.

Animals

Respiratory and postural changes in intercostal muscle length in supine dogs.

In an attempt to assess the physiological function(s) of the external (E) and internal interosseous (I) intercostal muscles, we measured the changes in intercostal muscle length during spontaneous breathing, during passive inflation, and during passive rotation of the trunk. Studies were performed on 46 muscles from 16 supine anesthetized dogs, and changes in muscle length were assessed by sonomicrometry. The changes were small during spontaneous breathing, whether before or after bilateral phrenicotomy, and the pattern was variable among animals and among interspaces. The E, however, particularly in the lower interspaces, often lengthened with inspiration, and the I, in particular in the upper interspaces, often shortened with inspiration. Only occasionally did the E and I in one interspace change in length in opposing directions. This was also true during passive inflation, where both E and I usually shortened in the upper interspaces and lengthened in the lower interspaces. By contrast, during passive rotation of the trunk, the E and I systematically changed in length in opposing directions, and either muscle could successively lengthen and shorten a substantial amount depending on the side of rotation. These results suggest that 1) the E and I in supine dogs do not behave as antagonistic muscles during moderate respiratory efforts; and 2) they do behave as antagonistic muscles during rotation of the trunk. A primary function of these muscles as rotators of the trunk, unlike breathing, may explain why two layers of intercostal muscles with different fiber orientation exist between the ribs.

Animals