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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↗

Bronchial stump reinforcement with the intercostal muscle flap without adverse effects.

OBJECTIVE: Bronchopleural fistula is a serious complication of pulmonary resection. For anatomical reasons, lower lobectomy is thought to carry a higher risk for bronchopleural fistula. We investigated the efficacy of bronchial stump reinforcement with a pedicled intercostal muscle flap after lower lobectomy and compared the responses in patients treated with the flap, without the flap, and with other types of flap. We also investigated whether harvesting the intercostal muscle flap leads to an increase in blood loss during surgery and whether the type of flap influences chest-tube volume and pain after surgery. METHODS: One hundred and sixty-eight patients had lower or middle-lower lobectomy between January 1990 and December 2004. The bronchial stumps were treated in one of the three ways: covered with an intercostal muscle flap (116 patients, group A), not covered with a muscle flap (32 patients, group B), or covered with free fat or pleura (20 patients, group C). In a separate study, we compared the blood loss during surgery, and chest-tube volume and pain after surgery between patients treated with the intercostal muscle flap (23 patients) and non-intercostal muscle flap (32 patients). RESULTS: No patients in group A exhibited bronchopleural fistula, and two patients in group B and one patient in group C exhibited bronchopleural fistula. These differences were not significant. Blood loss, chest-tube volume, and pain score after surgery did not differ significantly between treatment groups. CONCLUSIONS: Bronchial stump reinforcement with the intercostal muscle flap after pulmonary resection is safe and effective when performed during lower and lower-middle lobectomy and does not increase the risk of complications.

Adult↗

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.

Anesthetics, Local↗

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↗

Role of chemical drive in recruiting upper airway and inspiratory intercostal muscles in patients with obstructive sleep apnea.

Upper airway dilating muscle activity increases during apneic episodes in patients with obstructive sleep apnea (OSA). To elucidate the relative contribution of chemical and nonchemical stimuli to augmentation of the upper airway dilating muscle, we measured the response of genioglossus muscle (GG) and inspiratory intercostal muscle (IIM) activities to obstructive apnea during non-REM sleep and compared them with the response to progressive hypoxia and hypercapnia during awake periods in seven male patients with OSA. GG EMG was measured with a wire electrode inserted percutaneously, and IIM EMG was measured with surface electrodes placed in the second intercostal space parasternally. Responses to hypoxia and to hypercapnia were assessed by rebreathing methods in the supine position while awake. Following these measurements, a sleep study was conducted with the EMG electrodes placed in the same locations. The relationship between GG and IIM activities during the cycle of apnea and postapneic ventilation in non-REM sleep was quasi-linear, and the slope of the regression line was significantly greater than those during progressive hypoxia and progressive hypercapnia. The amplitude of GG activity at 70% of maximum IIM activities in the hypoxic test was 140 +/- 20% (mean +/- SEM) during non-REM sleep, which was also significantly greater than that during hypoxia (51 +/- 10%) and that during hypercapnia (59 +/- 15%). These results suggest that nonchemical factors contribute considerably to augmentation of GG activity during obstructive apneic episodes. The nonchemical stimuli may arise from mechanoreceptors activated by upper airway obstruction and behavioral factors associated with change in sleep states.

Adult↗

Intercostal muscle flap reduces the pain of thoracotomy: a prospective randomized trial.

BACKGROUND: Thoracotomy is associated with significant pain and morbidity. METHODS: We performed a prospective randomized trial over 4 months. Patients were randomized to a standard posterior-lateral thoracotomy or an identical procedure, except an intercostal muscle was harvested from the lower rib (to protect the intercostal nerve) before chest retraction. To ensure an equal distribution among both groups, patients were stratified by race, sex, and type of pulmonary resection. All patients received similar pain management. Pain was assessed by using multiple pain scores during hospitalization and after discharge. Outcomes assessed were pain scores, spirometric values, analgesic use, and activity level. RESULTS: There were 114 patients. The median time for intercostal muscle harvesting was 3.7 minutes. The numeric pain scores were lower for the intercostal muscle group on postoperative days 1 and 2 and at weeks 1, 2, 3, 4, 8, and 12 (P < .05 for all). In addition, patients in the intercostal muscle group had a smaller decrease in spirometric values, were less likely to be using analgesics, and were more likely to have returned to normal activity. CONCLUSIONS: The harvesting of an intercostal muscle flap before chest retraction decreases the pain of thoracotomy and leads to a lower decrease in spirometry. In addition, patients have less pain at 1, 2, 3, 4, 8, and 12 weeks postoperatively and are less likely to be using narcotics. Finally, it offers a pedicled muscle flap that takes little time to harvest and is able to buttress all bronchi after lobectomy.

Aged↗

Dynamic and static contributions to the rhythmic y activation of primary and secondary spindle endings in external intercostal muscle.

1. In cats anaesthetized with sodium pentobarbital 160 external intercostal muscle spindle afferents were identified by their pause in response to ventral root stimulation; the internal intercostal muscle was denervated. 2. In order to assignate the afferents to either primary or secondary endings they were tested for their responsiveness to vibration (Bianconi & Van Der Meulen, 1963). The maximal frequency which they were able to follow regularly for at least four cycles, termed 'critical frequency', was determined. 3. The endings fell into two groups: low-f (frequency) sensitive endings with critical frequencies below 400 c/s and high-f sensitive endings with critical frequencies above 400 c/s. The latter were regarded as primary endings and the former as secondary ones. 4. The manner in which the spindle endings resumed activity after a pause produced by shocks to the ventral root, i.e. whether 'phasic' or 'tonic' (Granit & Van Der Meulen, 1962) was studied in all the spindle afferents. 5. All the secondary (low-f sensitive) endings were 'tonic' except three for which the determination of critical frequency was questionable. Both 'tonic' and 'phasic' properties were found among the primary (high-f sensitive) endings. 6. The majority of the secondary endings (74%) showed inspiratory ythmic fusimotor activation in parallel with the skeletomotor contracton as did the primary endings (79 %). 7. Fifty-seven spindle endings which all showed marked rhythmic inspiratory gamma activation were tested for respiratory variations in their dynamic responses to steady stretch and length changes introduced at low repetition rates. 8. The results indicate that both 'dynamic' and 'static' gamma fibres are represented among the rhythmic gamma fibres controlling primary muscle spindle endings, whereas rhythmic activation of secondary endings seems to be mediated only by 'static' fibres.

Animals↗

Are the external and internal intercostal muscles synergist or antagonist in the cat?

The electrical activity of the external and internal intercostal muscles was recorded in decerebrated cats during eupnea and in the course of dyspnoea artificially induced to reinforce the inspiratory or expiratory central drive. In the cephalic part of the thorax (1st-5th ribs) the lateral part of the external and internal intercostal muscles are synergist and inspiratory. In the caudal part of the thorax (9th-13th ribs) these muscles are also synergist but expiratory. In the intermediate part (5th-9th ribs) the intercostal muscles are antagonist, the external ones are inspiratory and the internal ones are expiratory.

Animals↗

Spatial distribution of inspiratory drive to the parasternal intercostal muscles in humans.

The human parasternal intercostal muscles are obligatory inspiratory muscles with a diminishing mechanical advantage from cranial to caudal interspaces. This study determined whether inspiratory neural drive to these muscles is graded, and whether this distribution matches regional differences in inspiratory mechanical advantage. To determine the neural drive, intramuscular EMG was recorded from the first to the fifth parasternal intercostals during resting breathing in six subjects. All interspaces showed phasic inspiratory activity but the onset of activity relative to inspiratory flow in the fourth and fifth spaces was delayed compared with that in cranial interspaces. Activity in the first, second and third interspaces commenced, on average, within the first 10% of inspiratory time, and sometimes preceded inspiratory airflow. In contrast, activity in the fourth and fifth interspaces began after an average 33% of inspiratory time. The peak inspiratory discharge frequency of motor units in the first interspace averaged 13.4 +/- 1.0 Hz (mean +/- s.e.m.) and was significantly greater than in all other interspaces, in particular in the fifth space (8.0 +/- 1.0 Hz). Phasic inspiratory activity was sometimes superimposed on tonic activity. In the first interspace, only 3% of units had tonic firing, but this proportion increased to 34% in the fifth space. In five subjects, recordings were also made from the medial and lateral extent of the second parasternal intercostal. Both portions showed phasic inspiratory activity which began within the first 6% of inspiratory time. Motor units from the lateral and medial portions fired at the same peak discharge rate (10.4 +/- 0.7 versus 10.7 +/- 0.6 Hz). These observations indicate that the distribution of neural drive to the parasternal intercostals in humans has a rostrocaudal gradient, but that the drive is uniform along the mediolateral extent of the second interspace. The distribution of inspiratory neural drive to the parasternal intercostals parallels the spatial distribution of inspiratory mechanical advantage, while tonic activity was higher where mechanical advantage was lower.

Adult↗

Metabolism of perfused pig intercostal muscles evaluated by 31P-magnetic resonance spectroscopy.

This study presents a perfused preparation for evaluation of metabolism in pig intercostal muscle in vitro. Preserved vessels and nerves to an intercostal segment including two adjacent ribs allowed for tissue perfusion and electrical stimulation with measurement of contraction force, oxygen consumption and 31P-magnetic resonance spectroscopy (31P-MRS). When perfused at rest with Krebs-Ringer buffer, the preparation maintained physiological levels of phosphocreatine (PCr), inorganic phosphate (Pi), ATP and pH at a stable oxygen consumption of 0.51 +/- 0.01 micromol min(-1) g(-1) for more than 2 h. Tonic stimulation of the nerve caused anaerobic energy consumption as PCr and pH decreased, and both variables recovered after the contraction with half-time values of approximately 7 min. Force increased to 0.040 N g(-1) (range, 0.031-0.103 N g(-1)) and it gradually decreased by about 70% during the subsequent 5 min of stimulation. The calculated free ADP concentration increased from 7.4 +/- 2.1 nmol g(-1) at rest to 28 +/- 12 nmol g(-1) (mean +/- s.d.) by the end of the stimulation. Thus anaerobic ATP turnover was zero at rest, 6.1 +/- 2 micromol min(-1) g(-1) during the first minute of stimulation and 3.5 +/- 0.5 micromol min(-1) g(-1) during the two last minutes, corresponding to the drop in force. When the preparation was left unperfused, anaerobic ATP turnover averaged 0.40 +/- 0.15 micromol min(-1) g(-1) for the first 10 min. The preparation can also be applied to human intercostal muscles, as demonstrated in one preliminary experiment. The results demonstrate a stable and functional in vitro preparation of intact perfused intercostal muscles in the pig.

Adenosine Diphosphate↗

Glycogen depletion and lactate accumulation in human intercostal muscles after administration of succinylcholine.

I.m. glycogen content, lactate concentration and staining intensity for glycogen in slow- (ST) and fast-twitch (FTa and FTb) fibres were determined in the external and internal intercostal muscles after thoracotomy. Thirteen patients received a precurarizing dose of a non-depolarizing neuromuscular blocking agent followed by the depolarizing agent, succinylcholine, to facilitate intubation of the trachea (succinylcholine group). Nine patients received pancuronium or gallamine (control group). There were no significant differences in ventilatory functional capacity between the two groups. In the external intercostal muscles, lower i.m. glycogen content was observed in the succinylcholine compared with the control group (P < 0.05). I.m. glycogen was depleted from the FT fibres and in particular from FTb fibres, while little depletion was noted in ST fibres. In both the external and internal intercostal muscles, a higher lactate concentration was observed in the succinylcholine than in the control group (P < 0.05). The results indicate that the use of succinylcholine for tracheal intubation stimulated breakdown of i.m. glycogen, particularly in fast-twitch muscle fibres, and caused accumulation of lactate in intercostal muscles.

Adult↗

The proprioceptive reflex control of the intercostal muscles during their voluntary activation.

1. A quantitative study has been made of the reflex effects of sudden changes in mechanical load on contracting human intercostal muscles during willed breathing movements involving the chest wall. Averaging techniques were applied to recordings of electromyogram (EMG) and lung volume, and to other parameters of breathing.2. Load changes were effected for brief periods (10-150 msec) at any predetermined lung volume by sudden connexion of the airway to a pressure source variable between +/- 80 cm H(2)O so that respiratory movement could be either assisted or opposed. In some experiments airway resistance was suddenly reduced by porting from a high to a low resistance external airway.3. Contracting inspiratory and expiratory intercostal muscles showed a ;silent period' with unloading which is attributed to the sudden withdrawal from intercostal motoneurones of monosynaptic excitation of muscle spindle origin.4. For both inspiratory and expiratory intercostal muscles the typical immediate effect of an increase in load was an inhibitory response (IR) with a latency of about 22 msec followed by an excitatory response (ER) with a latency of 50-60 msec.5. It was established using brief duration stimuli (< 40 msec) that the IR depended on mechanical events associated with the onset of stimulation, whereas stimuli greater than 40 msec in duration were required to evoke the ER.6. For constant expiratory flow rate and a constant load, the ER of expiratory intercostal muscles increased as lung volume decreased within the limits set by maximal activation of the motoneurone pool as residual volume was approached.7. The ER to a constant load increased directly with the expiratory flow rate at which the load applied, also within limits set by maximal activation of the motoneurone pool.8. For a given load, the ER during phonation was greater than that occurring at a similar expiratory flow rate without phonation when the resistance of the phonating larynx was mimicked by an external airway resistance.9. It is argued that the IR is due to autogenetic inhibition arising from tendon organs and that the ER is due to autogenetic excitation arising from intercostal muscle spindles.10. The initial dominance of inhibition in this dual proprioceptive reflex control was not predicted by the servo theory. It is proposed that the reflex pathways subserving autogenetic inhibition are under a centrifugal control which determines in relation to previous experience (learning) the conditions under which autogenetic facilitation is allowed.

Airway Resistance↗

Lung function and surface electromyography of intercostal muscles in cement mill workers.

Impairment of pulmonary function in cement mill workers has been previously reported without considering a variety of parameters that can help evaluate more thoroughly the effect of cement dust on the respiratory system. In addition, an integrated approach has not been considered to assert the involvement of respiratory muscles. Therefore, in the present study spirometry and surface electromyography (SEMG) of intercostal muscles were used for indicating pulmonary impairment. In this study, a group of 50, apparently healthy volunteers, male cement mill workers aged 20-60 years with exposure of 13 years on average, were randomly selected. They were matched with another group of 50 control healthy male subjects in terms of age, height, weight and socioeconomic status. Both groups met the standard exclusion criteria. Spirometry was performed on an electronic spirometer, while SEMG of intercostal muscles was performed by using a chart recorder. The results demonstrated statistically significant reduction in lung function parameters i.e., force vital capacity (FVC) (p < 0.0005); force expiratory volume in first second (FEV1) (p < 0.0005); peak expiratory flow (PEF) (p < 0.005); and maximum voluntary ventilation (MVV) (p < 0.0005) in cement mill workers, when compared with controls. However, the FEV1/FVC ratio was significantly higher (p < 0.025) in cement mill workers. Similarly, the parameters obtained from SEMG of intercostal muscles, i.e. number of peaks (NOP) (p < 0.0005); maximum peak amplitude (MPA) (p < 0.0005); peak to peak amplitude (PPA) (p < 0.0005); duration of response (DOR) (p < 0.0005) and maximum peak duration (MPD) (p < 0.0005), were significantly lower in cement mill workers than in controls. It is concluded that exposure to cement dust not only impairs lung function but also affects costal muscle performance, thus possibly indicating the decreased lung and thoracic compliance.

Adult↗

[Comparison of several rib rings with intercostal muscles for tracheal replacement in dogs].

OBJECTIVE: To compare the effect of several types of rib rings with intercostal muscles for the replacement of trachea in thorax. METHODS: The surface layer of the third rib of dogs were ripped off and curved into triangular, quadrilateral and polygonal form. These three types of rib rings with intercostal muscles were used to replace a segment of trachea in thorax. RESULTS: The stability of triangular rib ring was very well, but stricture of ring were often happened because of its smaller internal diameter. These stability of quadrilateral rib ring was the worst. The polygonal rib ring presented the biggest diameter and good stability compared to the other two kinds of rings. If silicone tube was supplemented in the polygonal rib ring, the quality of artificial trachea was excellent. CONCLUSION: The rib rings with intercostal muscles are successfully used for replacing the defect of trachea in canine thorax. The polygonal rib rings have the best quality in the three types of rib ring for tracheal replacement.

Animals↗

Gas exchange during separate diaphragm and intercostal muscle breathing.

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

Animals↗

Electromyographic investigation of the diaphragm and intercostal muscles in tetraplegics.

Local electromyographic activity has been demonstrated in the intercostal muscles of tetraplegic patients by using a combination of surface, fine-wire and intra-oesophageal diaphragmatic electrodes. This activity is first present and most evident in the lower chest, the point of maximum deformation in the tetraplegic's thorax. In patients with long standing injury the activity is present and prominent in the more superior intercostal muscles. We believe this activity to be reflex in character and that it develops and facilitates over time, so improving the ventilatory capacity of tetraplegics.

Adult↗