Inspiratory Intercostal Muscles Research Articles

Inspiratory elevation of the ribs in the dog: primary role of the parasternals [published errata appear in J Appl Physiol 1991 Aug;71(2):following Table of Contents and 1991 Dec;71(6):following Author Index

To assess the relative contributions of the different groups of inspiratory intercostal muscles to the cranial motion of the ribs in the dog, we have measured the axial displacement of the fourth rib and recorded the electromyograms of the parasternal intercostal, external intercostal, and levator costae in the third interspace in 15 anesthetized animals breathing at rest. In eight animals, the parasternal intercostals were denervated in interspaces 1-5. This procedure caused a marked increase in the amount of external intercostal and levator costae inspiratory activity, and yet the inspiratory cranial motion of the rib was reduced by 55%. On the other hand, the external intercostals in interspaces 1-5 were sectioned in seven animals, and the reduction in the cranial rib motion was only 22%; the amount of parasternal and levator costae activity, however, was unchanged. When the parasternals in these animals were subsequently denervated, the levator costae inspiratory activity increased markedly, but the inspiratory cranial motion of the rib was abolished or reversed into an inspiratory caudal motion. These studies thus confirm that, in the dog breathing at rest, the parasternal intercostals have a larger role than the external intercostals and levator costae in causing the cranial motion of the ribs during inspiration. A quantitative analysis suggests that the parasternal contribution is approximately 80%.

Phrenic afferents and ventilatory control

It has been understood since the late 1800s that the diaphragm has significant sensory innervation. The role of phrenic afferents in the control of breathing, however, has been obscure. The phrenic nerve has been shown to contain a full array of afferent fibers. However, proprioceptive (group 1 fibers) afferents are few compared to postural muscles or the intercostals. The diaphragm, unlike the inspiratory intercostal muscles, has a small complement of spindle afferents and not all of these spindles are supplied with fusorial fibers. Reduced spindle afferents under gamma control help to explain previous studies of the diaphragm that have failed to reveal autogenic facilitation, that is, a reflex-mediated increase in drive during inspiratory loading. Nevertheless, some clinical studies have revealed increased activation of the diaphragm when its length is reduced. Group 1 fibers, which are predominantly tendon organ afferents in the diaphragm, have been shown to have a phasic inhibitory function. A reduction in this inhibition brought about by a reduction in diaphragmatic length during lung inflation may explain the increased diaphragmatic activation reported in clinical studies. Phrenic afferents have been shown to have multiple spinal and supraspinal projections. Recent studies have explored the ventilatory effects of thin fiber afferents (group III and IV fibers) in the phrenic nerve. Stimulation of these afferents has been shown both to inhibit and excite ventilation. These afferents arise from polymodal receptors that respond to both mechanical and chemical stimulation. Activation of these receptors may occur in a variety of conditions and the ventilatory response may be determined by the specific receptor activated.

Effects of inspiratory loading on 31phosphorus magnetic resonance (PMR) spectroscopy of the inspiratory intercostal muscles in normal humans

Effects of inspiratory loading on 31phosphorus magnetic resonance (PMR) spectroscopy of the inspiratory intercostal muscles in normal humans

Effects of Inspiratory Loading on 31Phosphorus Magnetic Resonance (PMR) Spectroscopy of the Inspiratory Intercostal Muscles in Normal Humans

Using the General Electric Signa magnetic resonance (MR) 1-m bore, 1.5-Telsa scanner, we assessed the changes in 31PMR spectroscopy of the inspiratory intercostal muscles in normal humans at rest and breathing inspiratory threshold loads to generate inspiratory mouth pressures at 25%, 50%, and 75% of maximum, the latter level designed to produce fatigue. Subjects were studied in the prone position overlying an 8-inch diameter surface coil positioned and secured over the anterior chest to incorporate the parasternal intercostal muscles.

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.

Inspiratory action of separate external and parasternal intercostal muscle contraction.

We have previously shown that electrical stimulation of the thoracic spinal cord produces near maximal activation of the inspiratory intercostal muscles. In the present investigation, we used this technique to evaluate the relative capacity of separate external (EI) and parasternal intercostal (PA) muscle contraction to produce changes in airway pressure and inspired volume. Studies were performed in 23 anesthetized phrenicotomized dogs. Electrical stimuli were applied to the spinal cord after hyperventilation-induced apnea, before and after sequentially severing either the PA or EI muscles from the first through sixth intercostal spaces. During spinal cord stimulation (SCS), measurements were made of inspired volume (delta V) with the airway open and negative airway pressure (delta P) during tracheal occlusion. Compared with control values, sectioning of the PA muscles resulted in a 40.9% reduction in delta P and 35.7% reduction in delta V during SCS. In other animals, initial sectioning of the EI muscles produced reductions in delta P and delta V of 67.4 and 63.0, respectively, during SCS. After subsequent section of the PA muscles, SCS produced only negligible inspired volumes and changes in airway pressure. We conclude that 1) the EI and PA muscles are each capable of generating substantial changes in airway pressure and large inspired volumes and 2) the ventilatory capacity of the EI muscles exceeds that of the PA muscles.

Histochemical characteristics of human expiratory and inspiratory intercostal muscles

The relative occurrence of slow-twitch (ST) and fast-twitch (FTa and FTb) fibers, fiber size, and capillary supply in internal (INT) and external intercostal muscles (EXT), the costal diaphragm (DIA), and vastus lateralis muscle (VAS) was examined post-mortem in eight healthy males. The relative occurrence of ST fibers in INT [64 +/- 3% (SE)] and EXT (62 +/- 3%) was similar but higher than in DIA (49 +/- 3%) and VAS (40 +/- 6%; P less than 0.05). The occurrence of FTa fibers in expiratory INT (35 +/- 3%) was higher than in inspiratory INT and EXT (17 +/- 1%; P less than 0.05) but similar to DIA (28 +/- 6%) and VAS (32 +/- 2%). Accordingly, expiratory INT had fewer FTb fibers (1 +/- 1%) than the others (P less than 0.05). Expiratory INT had a 60% larger fiber area than inspiratory INT and EXT and DIA (P less than 0.05), but the area was similar to that of VAS. The number of capillaries per fiber was higher in expiratory INT (2.3 +/- 0.1) than in inspiratory INT and EXT (1.6 +/- 0.1), DIA (1.9 +/- 0.1), and VAS (1.8 +/- 0.2; P less than 0.05). The results suggest that the occurrence of many large capillary-rich FTa fibers in expiratory INT is bound to function (expiratory vs. inspiratory) rather than to anatomy (INT vs. EXT).

Changes in neural drive (EMGd) and neuromuscular coupling during histamine-induced bronchoconstriction in patients with asthma

This study was undertaken in order to assess the neural drive to the respiratory muscles and the inspiratory neuromuscular coupling in patients with bronchial asthma during histamine-induced bronchoconstriction. Bronchoconstriction was produced in a graded fashion, with histamine phosphate aerosol of increasing dose, in twelve asymptomatic asthmatic patients and was measured by FEV1. Inspiratory drive was measured by electromyographic activity of the diaphragm (EMGd) and the coupling of the neural drive to the respiratory muscles was assessed by the relationship of mouth occlusion pressure (P0.1) to EMGd. During the test we also measured electromyographic activity of the inspiratory intercostal (EMGint), sternomastoid (EMGsm) and expiratory abdominal (EMGab) muscles. Histamine caused a significant decrease in FEV1, a significant increase in P0.1, EMGd, EMGint, and a relevant increase in EMGsm, with no substantial increase in EMGab. An inverse significant relationship between the change in FEV1 and changes in P0.1, EMGd and EMGint and a significant correlation between the change in FEV1 and in the P0.1/EMGd ratio were observed. We conclude that a progressive increase in bronchospasm is accompanied by a progressive increase in respiratory neural drive and decrease in neuromuscular coupling. This could be caused both by an increase in lung volume and a lack of abdominal expiratory muscle recruitment.

Maximal activation of the human diaphragm but not inspiratory intercostal muscles during static inspiratory efforts.

It is widely held that transdiaphragmatic pressure is a reliable index of the extent of central activation of the diaphragm but the maximal voluntary transdiaphragmatic pressure is lower during inspiratory than expulsive efforts. To determine whether the diaphragm is fully activated during the two manoeuvres supramaximal stimuli were delivered to both phrenic nerves during maximal efforts. No discernible twitch was evoked during 30-55% of attempted maximal efforts with either voluntary manoeuvre. Thus the difference in maximal transdiaphragmatic pressure between the manoeuvres must reflect changes in chest-wall geometry or mechanics rather than in the phrenic motor outflow. Inspiratory intercostal muscle activity was consistently submaximal during maximal inspiratory efforts.

Non-vagal reflex effects on medullary inspiratory neurons during inspiratory loading

Studies were conducted to compare the first-breath responses of medullary Dorsal and Ventral Respiratory Group inspiratory (I) neurons to the mechanical loading (tracheal occlusion, TO) of inspiration in unanesthetized (decerebrate) and anesthetized (Dial®) vagotomized cats, and to determine the sources of the sensory activity causing the changes in I-neuron activity. In decerebrate cats, TO resulted in a prolongation of the firing duration in 49% of the I-neurons. There was a delayed onset of firing in 7% of the I-neurons. The responses of I-neurons to TO in anesthetized cats were similar to the responses in decerebrate cats. Changes in I-neuron activity with TO were still present in cats with their cervical (C3-7) or thoracic (T1–9) dorsal roots cut, and absent when both cervical and thoracic dorsal roots were cut. The most probable sources of the cervical and thoracic afferent information altering medullary I-neuron activity during loading are the diaphgram and inspiratory intercostal muscles.

1797 AUGMENTED BREATHS (SIGHS): CHANGES IN THE RELATIVE CONTRIBUTION OF THE CHEST WALL AND ABDOMEN IN INFANCY

Electromyographic studies in animals suggest that the activation of the inspiratory intercostal muscles during augmented breaths is weaker in newborn animals compared to adults when simultaneous activation of diaphragm is compared. Since the relative contribution of these muscles during augmented breaths in neonates and children are not known, the present study was designed to determine the changes in abdominal and chest wall contribution during augmented breaths in newborn and in older infants. The abdominal and chest wall respiratory movements of ten newborn infants (<10 days) and 9 older infants (>6 weeks) were monitored by respiratory inductive plethysmograph bands. Spontaneous augmented breaths (sighs) in quiet sleep were analyzed. The control values were obtained from the mean of 3 breaths immediately preceding the augmented breath and the augmented breaths were expressed as percent of their controls. The increase in chest wall movement was smaller in newborn infants when compared to the increase in abdominal movement (173 vs 297%) whereas the increase in chest wall movement was greater in the older infants (426 vs 268%). These results suggest that the proprioceptive control of the chest wall muscles is immature in the neonatal period. This may result in poor compensation to added respiratory loads during the neonatal period. Supported by grants from the NIH (HL-01156) and the March of Dimes (5–426).

Intercostal muscle activity of the cat in the curled, semiprone sleeping posture

We examined the effect of different sleeping postures on intercostal muscle activity in the cat. Cats assume a variety of sleeping positions, but the semiprone, curled position with one side bearing most of the weight was the posture studied in these experiments. In this posutre the cat's head rests upon the forepaws and may be slightly tilted. A lateral and ventral curvature of the spine and a lateral flexion of the neck form a curl with an upward-concave side and a downward-convex side. We examined the differences in intercostal activity on the concave and convex sides in this semiprone curled position in seven adult cats. Activity was studied at 14 sites (7 showing inspiratory and 7 showing expiratory activity). Inspiratory intercostal muscle activity was in all cases greater on the concave-upward side; similarly, expiratory intercostal muscle activity was, with the exception of activity at one site, greater on the concave-upward side than on the convex downward side. This effect was evident in rapid-eye-movement (REM) as well as nonrapid-eye-movement (NREM) sleep.

Responses of upper airway, intercostal and diaphragm muscle activity to stimulation of oesophageal afferents in dogs.

The effects of oesophageal distension on respiratory patterns and the moving average electromyogram (e.m.g.) activity of three upper airway muscles--the alae nasi, the genioglossus, and the posterior cricoarytenoid--and four chest wall muscles--the costal and crural diaphragm and the inspiratory and expiratory intercostals--were examined in ten anaesthetized, tracheostomized, spontaneously breathing dogs. Distension was produced by inflations of a balloon placed in the middle part of the thoracic oesophagus with volumes of air ranging from 50 to 200 ml. Oesophageal distension increased respiratory frequency, mainly due to a significant shortening of the expiratory time. Activity of both the costal and crural parts of the diaphragm was inhibited with oesophageal distension, whereas that of the inspiratory intercostal muscles increased, tending to maintain a near-normal tidal volume and end-tidal CO2. Phasic inspiratory activity of all three upper airway muscles increased in response to oesophageal distension, as did the activity of the expiratory intercostal muscles. The changes in the breathing pattern and the electrical activity of all muscles in response to oesophageal distension were immediate, occurring during the first breath after the balloon was inflated. The responses were graded, so that increases in the volume of the oesophageal balloon progressively increased the activity of the upper airway and intercostal muscles, and decreased diaphragm activity. Bilateral vagotomy abolished the effects of oesophageal distension on upper airway and chest wall muscle activity, suggesting that vagal afferents constitute the major pathway for the reflex.

Role of intercostal muscles in the rib cage distortions produced by inspiratory loads.

We studied the patterns of rib cage (RC) deformation in six normal subjects breathing against different resistive and elastic inspiratory loads, and we examined, with concentric needle electrodes, the role played by the inspiratory intercostal muscles in the development of these patterns. Four of the subjects deformed their RC to a more elliptical shape during loaded inspirations; RC anteroposterior diameter became smaller and RC lateral diameter became larger. The RC deformation increased as the load increased, but it appeared to be independent of the nature of the load. Moreover these deformations were associated with a marked increase in the inspiratory activity of the intercostals situated in the lateral parts of the RC and a striking diminution of the activity in the parasternal area. On the other hand, two subjects invariably breathed along their RC relaxation characteristic, and they showed an increased inspiratory activity in all regions of the intercostal musculature. These findings indicate that 1) the pattern of RC deformation during loaded inspirations is closely related to the activity and coordination of the various inspiratory intercostal muscles, and 2) the parasternal intercostals are not necessarily representative of all the inspiratory intercostals. They are also strong evidence against the concept that the parasternal intercostal electrical activity normally recorded during quiet breathing is an excitatory reflex activity.

Effects of inspiratory loading on respiratory muscle activity during expiration.

We studied respiratory muscle activity during expiration in four normal subjects during inspiratory resistive and elastic loading, with and without positive and expiratory pressure. Net inspiratory muscle activity (Pmus) was measured by relating esophageal pressure to the chest wall relaxation pressure-volume (P-V) curve. Abdominal muscle activity (Pabd) was quantitated by relating gastric pressure to the relaxation P-V curve of the abdomen. The decay rates of Pmus and of transdiaphragmatic pressure (Pdi) were increased during loading, and end-expiratory lung volume decreased. The decay rates of Pmus and Pdi were inversely related to expiratory duration. Inspiratory intercostal/accessory activity during expiration was frequently observed together with Pabd, especially during elastic loading. We conclude that external mechanical loads, acting during inspiration, influence respiratory muscle behavior during expiration. Inspiratory loads diminish expiratory braking by the inspiratory muscles and recruit expiratory muscles. The rate of expiration is enhanced and its duration shortened. Simultaneous persistent action of the inspiratory intercostal and accessory muscles throughout expiration may serve to optimize diaphragmatic length.

Inspiratory muscle activity during rebreathing in intact and vagotomized rabbits

The relation between relative peak ‘integrated’ diaphramagmatic (Adi) and cranial (u) or caudal (1) inspiratory intercostal activity (Aic) was assessed in intact and vagotomized rabbits during rebreathing. During unloaded rebreathing Aic increased markedly more than Adi, and Aic u more than Aic l, independently of intact vagi. Vagal signals facilitated inspiratory intercostals, since vagotomy or vagal blocks increased Adi more than Aic without changing diaphargm acitivity time course, and ΔAic/ΔAdi in the same range of Adi values was greater before than after vagotomy. Reflexes from the chest wall were not involved since phrenic block after vagotomy modified rib cage motion without changin Aic, independently of chemical drive. Possibly chemical and vagal dependent changes in fusimotor activity are responsible for greater Aic increase, which in turn explains the decreasing relative diaphragm contribution of V t, as the latter increases. Obstruction at FRC shifted postvagotomy Aic vs. Adi relationship upwards, suggesting reflex facilitation of intercostals by chest wall receptors. The strength of this reflax was largely independent of intact vagi, since pre- and postvagotomy Aic vs. Adi relations coincided, and of chemical drive, since postvagotomy ΔAic/ΔAdi for obstructed and unimpeded rebreathing were similar.

The Role of Respiratory Muscles in the Hyperinflation of Bronchial Asthma1–3

To examine the mechanism of hyperinflation in bronchial asthma we studied lung and chest wall mechanics in 7 asymptomatic patients in whom progressive bronchoconstriction was induced by doubling the amount of inhaled aerosolized histamine. An increase in pulmonary resistance (RL) from 2.5 +/- 0.3 cmH2O . 1-1 . s (mean, +/- 1 SE) to 12.3 +/- 0.9 cmH2 was associated with a linear increase in functional residual capacity (FRC) up to 74.7 +/- 1.7% of control total lung capacity (TLCc). The mean regression coefficient was 2.3% TLCc . cmH2O-1 . 1 . s-1. At each level of hyperinflation the most positive expiratory pleural pressures measured during spontaneous breathing were generally less than the predicted chest wall relaxation pressures, indicating persistent inspiratory muscle contraction throughout expiration. This was predominantly due to inspiratory intercostal and accessory muscle activity, because measurements of transdiaphragmatic pressure indicated complete diaphragmatic relaxation early in expiration. Recruitment of abdominal muscles during expiration, inferred from measurements of gastric pressure (Pg) and abdominal antero-posterior (A-P) diameter, was progressively more apparent with increasing bronchoconstriction. We concluded that the increase in FRC in induced asthma is substantially influenced by persistent inspiratory intercostal and accessory muscle activity during expiration. Concomitant abdominal muscle recruitment results in a chest wall configuration that tends to optimize diaphragmatic function.

The interaction between the diaphragm, intercostal/accessory muscles of inspiration and the rib cage

During Mueller maneuvers (MM), the volume change of rib cage, ΔVrc, and abdomen, ΔVab, are equal and opposite. Thus ΔVrc = ΔVab. Substituting ΔPrc · Crc for ΔVrc and ΔPab · Cab for ΔVab yields: ΔPrc = − ΔPab · Cab/Crc, where ΔPrc, ΔPab, Crc and Cab are applied pressures and compliances of rib cage and abdomen respectively. MM performed solely with the diaphragm permits calculatins of Prc in terms of observed changes in Pab and pleural pressure, Ppl. Three trained subjects performed MM with no evidence of inspiratory intercostal or abdominal muscle contraction. During the diaphragmatic MM ΔPab was positive and ΔPrc negative. The magnitude of ΔPrc/ΔPab was 2–6 times greater than that of ΔPpl/ΔPab. We conclude that neither Pab nor Ppl by themselves displace the relaxed rib cage during Mueller maneuvers. A model in which the diaphragm acts both in parallel and in series with the rib cage, and in which Prc is the sum of Pab and a pressure lying between Pab and Ppl explains these results as well as the hypothesis that Pab displaces the relaxed rib cage during quiet breathing.

Role of Selected Muscles of Respiration as Influenced by Posture and Tidal Volume

Studies of the activity of accessory respiratory muscles were conducted in 30 normal subjects (15 male and 15 female subjects, age 5 to 62 years). Electromyograms were recorded over the right serratus anterior muscle and the adjacent sixthe intercostal space, and the results were correlated with tidal volume. Phasic respiratory activity in the serratus anterior muscle was detected in every subject but was markedly affected by the prevailing posture and level of ventilation (appearing at mean tidal volumes equivalent to 60.5 percent of vital capacity when subjects were standing relaxed, and equivalent to 35.2 percent of vital capacity when subjects were seated, leaning forward with elbows supported). The activity was predominantly inspiratory in timing but in some subjects extended into early expiration. No significant differences were noted in subjects of different ages, sex, height, or weight. Similar results were recorded from the inspiratory intercostal muscle. On the basis of these findings, we conclude that, contrary to reports, the serratus anterior muscle should be classified as an accessory muscle of respiration, at least at increased levels of ventilation, and that its activity is most pronounced in postures that place the muscles' origin in an advantageous position for moving the ribs.

The role of the fusimotor system with respect to the contribution of the diaphragm and the intercostal muscles to the respiratory tidal volume.

The efferent electrical activity in the phrenic nerve can be quantified in such a way that it gives a good correlation to tidal volume. After administration of the drug benzoctamine this relationship changes: more phrenic nerve activity is needed for the same tidal volume. No changes were found in the neuro-muscular transmission from the phrenic nerve to the diaphragm. There was no alteration in dynamic compliance of the lungs or in airway resistance. The afferent phrenic nerve activity from proprioceptors in the diaphragm did not change. It seems unlikely that respiratory neurons in the brainstem were affected since the sensitivity of the respiratory system to CO2 did not change. It is known that the tonic fusimotoneuron activity is suppressed at a supraspinal level by benzoctamine. Since intercostal muscles have muscle spindles and the diaphragm hardly has any, the intercostal muscle activity will be affected more than diaphragmatic activity by benzoctamine. This could actually be shown by quantifying the electromyogram of inspiratory external intercostal muscles. The tidal volume regulation is controlled by the vagal feedback loop. In order to reach a certain tidal volume after administration of benzoctamine, the contribution of the diaphragm has to increase because the activity of the intercostal muscles is diminished.