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J Physiol (2003), 548.1, pp. 297-305
© Copyright 2003 The Physiological Society
DOI: 10.1113/jphysiol.2002.032912
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ABSTRACT |
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High-frequency mechanical vibration of the ribcage increases afferent activity from external intercostal muscle spindles, but the effect of this procedure on the mechanical behaviour of the respiratory system is unknown. In the present study, we have measured the changes in external intercostal muscle length and the craniocaudal displacement of the ribs during ribcage vibration (40 Hz) in anaesthetized dogs. With vibration, external intercostal inspiratory activity increased by ~50 %, but the respiratory changes in muscle length and rib displacement were unaltered. A similar response was obtained after the muscles in the caudal segments of the ribcage were sectioned and the caudally oriented force exerted by these muscles on the rib was removed, thus suggesting that activation of external intercostal muscle spindles by vibration generates little tension. Prompted by this observation, we also examined the role played by the external intercostal muscle spindles in determining the respiratory displacement of the ribs during breathing against high inspiratory airflow resistances. Although resistances consistently elicited prominent reflex increases in external intercostal inspiratory activity, the normal inspiratory cranial displacement of the ribs was reversed into an inspiratory caudal displacement. Also, this caudal rib displacement was essentially unchanged after section of the external intercostal muscles, whereas it was clearly enhanced after denervation of the parasternal intercostals. These findings indicate that stretch reflexes in external intercostal muscles confer insufficient tension on the muscles to significantly modify the mechanical behaviour of the respiratory system.
(Received 20 September 2002; accepted after revision 19 January 2003; first published online 7 March 2003)
Corresponding author A. De Troyer: Chest Service, Erasme University Hospital, 808 Route de Lennik, 1070 Brussels, Belgium. Email: a-detroyer{at}yahoo.fr
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INTRODUCTION |
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Although medical treatment of airflow obstruction has made significant progress, dyspnoea remains a major cause of disability in many patients with chronic obstructive pulmonary disease. Studies, however, have shown that this symptom could be relieved by the application of high-frequency mechanical vibration to the parasternal region of the ribcage during inspiration (Sibuya et al. 1994; Christiano & Schwartzstein, 1997). Vibration of the parasternal region has also been shown to reduce the sense of effort in healthy subjects breathing CO2-enriched gas mixtures or breathing against inspiratory resistive loads (Manning et al. 1991; Edo et al. 1998). Because high-frequency vibration is a potent stimulus of spindle primary endings in limb muscles (Brown et al. 1967; Burke et al. 1976), this beneficial effect on dyspnoea has been primarily attributed to increased afferent information from the intercostal muscles. The actual effects of ribcage vibration on the respiratory system, however, are still uncertain.
To approach this problem, we have examined the electrical response to vibration of the inspiratory intercostal muscles in a group of anaesthetized dogs (Leduc et al. 2000). When vibration was applied during hyperventilation-induced apnoea, the internal intercostal muscles of the parasternal region (the so-called parasternal intercostals) showed occasional, low-amplitude electrical activity. In contrast, a prominent activity was consistently recorded from the external intercostal muscles in the rostral segments. Similarly, when vibration was applied during the inspiratory phase of the breathing cycle, there was a substantial increase in external intercostal inspiratory activity but no alteration in parasternal intercostal inspiratory activity (Leduc et al. 2000). Thus the external intercostals are much more sensitive to vibration than the parasternal intercostals, and this difference is fully consistent with the known difference in spindle density between the two muscle groups. Indeed, histological studies of intercostal muscles in cats (Duron et al. 1978) and electrophysiological studies in dogs (De Troyer, 1991a, 1996) have clearly established that the external intercostal muscles are abundantly supplied with muscle spindles and that the parasternal intercostals are poorly endowed.
The present studies were initially undertaken to assess the effects of ribcage vibration on the mechanical behaviour of the canine external intercostal muscles during breathing. Sensitive indices of this behaviour, in particular the changes in muscle length and the craniocaudal displacement of the ribs, were measured. Although external intercostal inspiratory activity was increased during vibration, these indices showed no alteration. The hypothesis was raised, therefore, that the magnitude of spindle stimulation during this procedure was insufficient to affect the mechanics of the respiratory system; or, alternatively, muscle spindles in the external intercostals were adequately activated by vibration but their mechanical effects are small. Therefore, to differentiate between these possibilities, we subsequently examined the action of the external intercostals in conditions known to induce strong stimulation of intercostal muscle spindles, i.e. during breathing against elevated inspiratory airflow resistance and during airway occlusion (Corda et al. 1965; Sant'Ambrogio & Widdicombe, 1965; Shannon & Zechman, 1972; De Troyer, 1992).
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METHODS |
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The experiments were carried out on 15 adult mongrel dogs (13-23 kg), as approved by the Animal Ethics and Welfare Committee of the Brussels School of Medicine. The animals were anaesthetized with pentobarbitone sodium (initial dose, 25 mg kg-1 I.V.), placed in the supine posture, and intubated with a cuffed endotracheal tube. A venous cannula was inserted in the forelimb to give maintenance doses of anaesthetic, and a catheter was inserted in the right femoral artery to monitor blood pressure and sample arterial blood periodically for blood gas analysis. The ribcage and intercostal muscles were then exposed from the first to the tenth rib by deflection of the skin and underlying muscle layers, after which two experimental protocols were followed.
Experiment 1
The mechanical response of the external intercostal muscles to ribcage vibration was studied in six animals. In each animal, we recorded the respiratory changes in length of the external intercostal muscle in the third right interspace and the craniocaudal (axial) displacement of the fourth rib. The displacement of the rib was measured with a linear displacement transducer (Schaevitz Eng., Pennsauken, NJ, USA) connected to a hook inserted into the rib in the midaxillary line, and the changes in muscle length were measured with a pair of piezoelectric crystals (2 mm diameter) implanted 6-10 mm apart in a well-identified muscle bundle and connected to a sonomicrometer (Triton Technology, San Diego, CA, USA). Detailed descriptions of these two techniques have been given in previous reports (De Troyer & Kelly, 1982; Newman et al. 1984; De Troyer, 1992).
In addition, in each animal we recorded the electromyograms of the external intercostal and parasternal intercostal muscles in the third right interspace with pairs of stainless-steel hook electrodes spaced 3-4 mm apart. Each electrode pair was placed in parallel fibres and inserted in the area of the muscle that receives the greatest inspiratory neural drive. The parasternal intercostal electrodes were thus inserted in the portion of the muscle close to the sternum (De Troyer & Legrand, 1995), and the external intercostal electrodes were inserted in the dorsal portion of the muscle, 1-2 cm ventral to the rib angle and 1 cm dorsal to the piezoelectric crystals (Kirkwood et al. 1982; Greer & Martin, 1990; Legrand & De Troyer, 1999). The two electromyographic (EMG) signals were processed using amplifiers (CWE, model 830/1, Ardmore, PA, USA), bandpass filtered below 100 and above 2000 Hz, and rectified prior to their passage through leaky integrators with a time constant of 0.2 s.
The animal was allowed to recover for 30 min after instrumentation, after which it was connected to a heated Fleisch pneumotachograph and a differential pressure transducer (Validyne, Northridge, CA, USA) for the measurement of lung volume. The animal was spontaneously breathing throughout. Every five to ten breaths, however, trains of vibration were applied for one breath first to the parasternal intercostal muscle in the fourth interspace, then to the parasternal intercostal muscle in the second interspace. The vibrations were delivered by a commercially available electromagnetic vibrator (LDS, model V. 101; Royston, Herts, UK) which was held manually, perpendicular to the muscle, so that the site and the force of application could be well controlled; the area of contact between the vibrator and the muscle was ~1.8 cm2. Since the muscle was vibrated perpendicularly, rather than longitudinally, the vibrations were attenuated and the changes in muscle length were much smaller than the movement of the moving element of the vibrator (Leduc et al. 2000). Also, the relation between the frequency of vibration and the amplitude of movement of this element was such that for a constant input voltage, the movement was greatest when the frequency was 40-50 Hz. Therefore, to induce significant ribcage vibration and elicit widespread stimulation of external intercostal muscle spindles, the vibrator in each animal of the study was adjusted so that the amplitude and the frequency of vibration was 2-2.5 mm and 40 Hz, respectively. Indeed, when such vibrations are applied to the parasternal intercostal muscle in a particular segment of the ribcage in the dog, spindles in the ventral portion of the external intercostal close to the site of vibration are triggered, but spindles in the dorsal portion of the muscle in the same segment and those in the dorsal portion of the external intercostals in many distant segments are triggered as well (Leduc et al. 2000).
The investigator received continuous feedback of parasternal intercostal EMG activity via a loudspeaker, and vibrations were applied exclusively during the inspiratory phase of the breathing cycle (in-phase). They were thus initiated concomitantly with or just before the onset of parasternal intercostal activity and maintained until the onset of the expiratory pause. At least 10 breaths with in-phase vibration of the parasternal intercostal muscle in the fourth interspace and 10 breaths with in-phase vibration of the parasternal intercostal in the second interspace were recorded in each animal. The external intercostal and levator costae muscles in the fourth to seventh right interspaces were subsequently sectioned from the costochondral junctions to the spine, and after a recovery period of 15 min, vibration of the parasternal intercostal muscle in the second interspace was repeated.
Experiment 2
The mechanical action of the external intercostal muscles during breathing against inspiratory resistive loads and during airway occlusion was studied in nine animals. The electromyograms of the external intercostal and parasternal intercostal muscles in the third right interspace and the axial displacement of the fourth rib were measured as described in Experiment 1. In addition, the changes in pleural pressure (Ppl) were obtained with a conventional balloon-catheter system placed in the middle third of the oesophagus and filled with 0.5 ml of air.
As in Experiment 1, the animal was breathing spontaneously throughout. At regular intervals, however, a resistor was added to the inspiratory line of a Hans-Rudolph valve attached to the pneumotachograph. Four different resistors were used. These were 1 cm long Plexiglass cylinders through which holes of 4, 3, 1.75 and 1 mm had been bored, and they will be referred to here as R1, R2, R3 and R4, respectively. The resistor was always added during the expiratory pause and left on for a single inspiratory effort, so we could investigate the neural reflex response to loading and its mechanical correlate before significant changes in chemical respiratory drive had developed. Each resistor was added at least three times in each animal. Four to six occluded breaths separated by 10 to 15 unimpeded breaths were also obtained.
After completion of these measurements, the external intercostal and levator costae muscles in all interspaces from the first to the seventh were severed on both sides of the chest, and the procedure was repeated. As during control, at least three trials with each resistor and four occluded breaths were obtained in this condition. Finally, the internal intercostal nerves in all interspaces from the first to the seventh were exposed at the chondrocostal junctions on both sides of the chest, and the nerves were sectioned to inactivate the parasternal intercostal muscles. Inactivation of the muscle in each interspace was confirmed by abolition of the inspiratory EMG activity. A last set of measurements was then performed.
The animals in both experiments appeared to remain at a satisfactory depth of anaesthesia throughout. They did not react to painful stimuli and made no spontaneous movements other than respiratory movements both during surgery and during the measurements. Since deep anaesthesia might have affected the responses of the external intercostal muscles to vibration and to inspiratory resistive loading, the level during measurements, however, while still sufficient to prevent the pupillary light reflex and the flexor withdrawal of the forelimbs in response to passive extension, did not inhibit the corneal reflex; whenever the animals showed a flexor withdrawal of the forelimbs or a pupillary light reflex, they were given a small, additional dose of anaesthetic (1-2 mg kg-1 I.V.). Also, rectal temperature was kept constant between 36 and 38 °C with infrared lamps. At the end of the experiment, the animals were given an overdose of anaesthetic (30-40 mg kg-1 I.V.) and postmortem examination of the ribcage was performed. It confirmed that the external intercostal and levator costae muscles in the fourth to the seventh right interspaces had indeed been severed entirely in each animal of Experiment 1. Similarly, six of nine animals of Experiment 2 showed complete section of the muscles in all interspaces on both sides of the chest. In the other three animals, a few deep muscle bundles had been left in the most dorsal portion of the first two interspaces.
Data analysis
In each animal, the changes in parasternal intercostal and external intercostal inspiratory activity during vibration (Experiment 1) and during inspiratory resistive loading (Experiment 2) in each condition were first quantified by measuring the peak height of the integrated EMG signals during each vibrated (or loaded) breath and during the immediately preceding non-vibrated (or unloaded, control) breath. To allow comparison between the different animals, EMG activity during vibrated and loaded breaths was then expressed as a percentage of the activity recorded during the control breaths. The duration of inspiration (inspiratory time, TI), defined as the period beginning at the onset of the parasternal inspiratory burst and concluding with peak parasternal activity, did not show any consistent alteration with vibration. However, during inspiratory resistive loading, TI increased gradually as the load was greater. Therefore, analysis of EMG recordings in Experiment 2 was also made by superimposing, in each animal, the traces of integrated signals obtained during each loaded breath on the traces obtained during the immediately preceding unimpeded breath (Younes et al. 1975; van Lunteren et al. 1984; Strohl, 1985; De Troyer, 1991a, 1992). For each muscle, activity during the loaded breath was calculated at the peak parasternal activity during the unloaded breath, and the amount of facilitation or inhibition during loading was defined as follows:
(EMG activity during the loaded breath/EMG activity during the unloaded breath) 
100 %.
The axial displacement of the rib during inspiration was expressed in millimetres and measured relative to the relaxation position of the rib, as determined during hyperventilation-induced apnoea. Similarly, the inspiratory changes in external intercostal muscle length were measured relative to the relaxation length (Lr) of the muscle, although they were expressed as percentage changes relative to Lr. The passive cranial motion of the ribs and the passive shortening of the external intercostal muscles that relaxation of the expiratory muscles commonly induces at the end of expiration (De Troyer & Ninane, 1986) were thus discarded from the study's calculations. The data analysis also discarded the transient, abrupt cranial motion of the rib and the transient, abrupt shortening of the external intercostal muscles that are occasionally seen after the cessation of inspiration and are related to the elastic recoil properties of the ribcage (De Troyer & Farkas, 1990). The changes in muscle length and the axial rib motion during vibration (Experiment 1), therefore, were measured at the peak tidal volume, and the changes during inspiratory resistive loading (Experiment 2) were measured at the peak pleural pressure. By convention, these two variables were assigned a positive sign when the muscle lengthened beyond Lr and the rib moved in the cranial direction; they were assigned a negative sign when the muscle shortened below Lr and the rib moved in the caudal direction.
The electrical activity in each muscle, the inspiratory displacement of the rib, and the inspiratory changes in external intercostal muscle length in each animal were obtained by averaging the responses to all vibrated and all loaded breaths. Data were then averaged over the different animals, and they are presented as means ± S.E.M. Statistical assessments of the effects of vibration were made by using Student's paired t tests. Assessments of the effects of graded inspiratory resistances in the different conditions were made by analysis of variance (ANOVA) with repeated measures and multiple comparison testing of the mean values performed, when appropriate, using Student-Newman-Keul's tests. The criterion for statistical significance was taken as P < 0.05.
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RESULTS |
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Response to ribcage vibration (Experiment 1)
The animals had a mean arterial pressure of CO2 (PCO2) of 41.6 ± 2.1 mmHg and a mean arterial PO2 of 85.2 ± 4.0 mmHg. The effects of in-phase vibration of the fourth interspace on the EMG activity and the changes in length of the external intercostal muscle in the third interspace and the axial displacement of the fourth rib are illustrated by the records of a representative animal in Fig. 1. Vibrating the fourth interspace during inspiration did not induce any alteration in parasternal intercostal activity but elicited a consistent increase in external intercostal activity in every animal. For the animal group, whereas parasternal intercostal activity in the vibrated breaths was 105 ± 2 % of the activity in the control breaths (NS), external intercostal activity thus amounted to 159 ± 12 % (P < 0.005). However, the phasic inspiratory cranial displacement of the rib amounted to 1.87 ± 0.53 mm during the control breaths and remained unchanged at 1.75 ± 0.49 mm (NS) during the vibrated breaths. The phasic inspiratory shortening of the external intercostal muscle (control, -2.75 ± 1.16 % Lr; vibration, -2.01 ± 0.85 % Lr; NS) and tidal volume (control, 332 ± 32 ml; vibration, 339 ± 34 ml; NS) remained also unchanged. Similarly, with vibration of the second interspace, peak external intercostal activity in the six animals increased to 149 ± 14 % of the activity in the control breaths (P < 0.02), but the inspiratory cranial displacement of the rib (control, 1.91 ± 0.55 mm; vibration, 1.82 ± 0.59 mm; NS), the inspiratory shortening of the muscle (control, -2.62 ± 1.19 % Lr; vibration, -2.43 ± 1.12 % Lr; NS) and tidal volume (control, 330 ± 36 ml; vibration, 321 ± 36 ml, NS) were unaltered.
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Figure 1. Response of intercostal muscles to ribcage vibration Traces of electrical activity (integrated signal) of the parasternal and external intercostal muscles (third interspace), changes in length of the external intercostal muscle, and axial motion of the fourth rib are shown for one representative animal. The changes in muscle length are expressed as percentage changes relative to the relaxation length (Lr). In the absence of vibration, the parasternal and external intercostal muscles are electrically active during the inspiratory phase of the breathing cycle; concomitantly, the external intercostal muscle shortens (downward deflection) and the rib moves cranially (upward deflection). Vibration (40 Hz) induces an increase in external intercostal activity. However, the inspiratory shortening of the muscle and the inspiratory cranial motion of the rib remain unchanged. | ||
Sectioning the external intercostal and levator costae muscles in the fourth to the seventh interspaces had no effect on the electrical or the mechanical response to vibration of the external intercostal muscle in the third interspace. Thus, when vibration was applied to the second interspace in this condition, peak external intercostal inspiratory activity increased to 143 ± 10 % of the activity in the non-vibrated breaths (P < 0.02) but the inspiratory muscle shortening was still unchanged (control, -2.72 ± 1.45 % Lr; vibration, -2.76 ± 1.47 % Lr; NS). The inspiratory cranial displacement of the fourth rib (control, 2.41 ± 0.78 mm; vibration, 2.29 ± 0.72 mm; NS) and tidal volume (control, 300 ± 29 ml; vibration, 292 ± 29 ml; NS) also remained unchanged.
Response to increased inspiratory resistance (Experiment 2)
The effects of adding an inspiratory resistance for a single breath on the EMG activity of the parasternal and external intercostal muscles and the axial displacement of the ribs are illustrated by the records of a representative animal in Fig. 2, and the changes observed with the different resistances in the nine animals are summarized in Figs 3-5. When the integrated EMG signals recorded during the loaded and unloaded breaths were superimposed, such that the influence of inspiratory duration was eliminated, external intercostal activity showed a gradual facilitation as the load increased (P < 0.05) (Fig. 3A and B) whereas parasternal intercostal activity showed a small inhibition or no change. As a result, although the two muscles gradually increased their peak EMG activity (P < 0.001), peak external intercostal activity during airway occlusion amounted to 631 ± 240 % of the activity recorded in the unloaded breaths (Fig. 3C), but peak parasternal intercostal activity was only 125 ± 5 % (Fig. 3D).
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Figure 2. Example of the changes in intercostal EMG activity and axial rib motion during breathing against an increased inspiratory resistance Same conventions as in Fig. 1. During unimpeded breathing, the parasternal and external intercostal muscles (third interspace) are electrically active during inspiration and the fourth rib moves cranially. With the addition of an inspiratory resistance (arrows), external intercostal activity increases markedly. However, the inspiratory cranial motion of the rib is reversed into an inspiratory caudal motion. The resistance applied here was resistor 4 (R4). Ppl, pleural pressure. | ||
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Figure 3. Electrical response of intercostal muscles to increased inspiratory resistance A, superimposed traces of electrical activity (integrated signal) of the parasternal and external intercostal muscles during an unimpeded breath (dotted lines) and a loaded breath (continuous lines) in one representative animal (same animal as in Fig. 2). Comparison of activity at peak parasternal activity (vertical line) shows a facilitation of external intercostal activity during the loaded breath and a small inhibition of parasternal activity. B, mean ± S.E.M. values of external intercostal (int) activity at peak parasternal activity during breathing against four graded resistors (R1-R4) and during airway occlusion (Occl) in nine animals. C, mean ± S.E.M. values of peak external intercostal inspiratory activity during loaded breaths. D, mean ± S.E.M. values of peak parasternal intercostal activity during loaded breaths before (open bars) and after (filled bars) section of the external intercostal muscles. Data in C and D are expressed as percentages of the peak activity during unimpeded breaths (control) before muscle section. | ||
As shown in Fig. 4, however, these increases in inspiratory EMG activity were associated with a gradual reduction in the inspiratory cranial displacement of the ribs (P < 0.001). In eight animals, high resistances and airway occlusion even reversed the normal inspiratory cranial displacement into an inspiratory caudal displacement. For the nine animals, therefore, whereas the inspiratory axial rib motion during unloaded breathing averaged +2.77 ± 0.32 mm, during airway occlusion, it was -1.56 ± 0.48 mm. Concomitantly, there was a gradual increase in 
Ppl (P < 0.001) (Fig. 5).
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Figure 4. Effect of increased inspiratory resistance on axial rib motion Mean ± S.E.M. values of inspiratory axial rib motion during unimpeded breathing (control, C), during breathing against four graded resistors (R1-R4), and during airway occlusion obtained in nine animals with intercostal muscles intact ( | ||
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Figure 5. Effect of increased inspiratory resistance on Ppl Mean ± S.E.M. data from nine animals. Same conventions as in Fig. 4. | ||
Sectioning the external intercostal muscles in all interspaces on both sides of the chest did not alter the inspiratory cranial displacement of the ribs during unloaded breathing (Fig. 4). Also, the inspiratory cranial displacement of the ribs continued to decrease progressively as the load increased, and although rib displacement in this condition was less cranial or more caudal than before muscle section, the differences were small and did not reach the level of statistical significance. For any given load, however, peak parasternal intercostal EMG activity (Fig. 3D) and Ppl (Fig. 5) after muscle section were similar to those measured with the muscles intact.
On the other hand, denervating the parasternal intercostal muscles had a dramatic effect on the inspiratory axial displacement of the ribs (P < 0.001). As shown by the records of a representative animal in Fig. 6, the ribs in this condition moved consistently in the caudal direction during unloaded breathing, and this caudal displacement increased as the load was increased. During airway occlusion, therefore, whereas the inspiratory displacement of the ribs after section of the external intercostals was -2.41 ± 0.34 mm, after denervation of the parasternal intercostals, it amounted to -4.46 ± 0.52 mm (P < 0.001) (Fig. 4). The Ppl values after denervation of the parasternal intercostals, however, were smaller than those after section of the external intercostals (P < 0.001) (Fig. 5).
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Figure 6. Example of respiratory displacement of the ribs after denervation of the parasternal intercostals Same animal and same conventions as in Fig. 2. The external intercostal muscles in all interspaces had previously been severed, so both the external intercostals and the parasternal intercostals are electrically silent. Note the inspiratory caudal displacement of the rib during unimpeded breathing and the increased caudal displacement with the addition of an inspiratory resistor (R4). | ||
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DISCUSSION |
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The present studies have confirmed the previous observation that high-frequency vibration of the ribcage during inspiration elicits an increased inspiratory activity in the canine external intercostal muscles without causing any change in the activity of the parasternal intercostals (Leduc et al. 2000). These studies, however, have also established that vibration does not alter the inspiratory shortening of the muscles or the inspiratory displacement of the ribs. This lack of alteration implies that stimulation of external intercostal muscle spindles by vibration has no significant impact on the mechanical behaviour of the ribcage, and although it pertains to dogs, rather than humans, it further suggests that the relief of dyspnoea observed in subjects with chronic obstructive pulmonary disease (Sibuya et al. 1994; Christiano & Schwartzstein, 1997) is not related to the mechanics of the respiratory system.
The finding that the increased inspiratory activity in the external intercostal muscle of the third interspace did not result in an increased inspiratory muscle shortening and an increased inspiratory cranial displacement of the fourth rib, does not necessarily mean that the force exerted by this particular muscle on the rib was unchanged. Indeed, as we have pointed out (see Methods), vibrations such as those used in the current study elicit widespread stimulation of external intercostal muscle spindles (Leduc et al. 2000). In our animals, therefore, when the vibrator was applied to the parasternal intercostal muscle in the fourth interspace, external intercostal inspiratory activity was increased in the third interspace, but external intercostal activity must also have been increased in many interspaces caudal to the fourth rib. Since the force exerted on the rib by these muscles is oriented caudally, this increased caudal activity might obscure the effects of the external intercostals in the three rostral interspaces on the inspiratory rib displacement and the inspiratory muscle shortening. It is most likely that external intercostal inspiratory activity in the fourth and fifth interspaces was also increased when the vibrator was applied to the parasternal intercostal muscle in the second interspace.
To test the importance of this mechanism, we sectioned the muscles in all caudal segments, such that the force developed by the muscles in the rostral segments was left unopposed. When the ribcage was vibrated in this condition, no increase in inspiratory muscle shortening or in cranial rib motion appeared, thus indicating that the external intercostal muscles caudal to the segment being investigated were not a determining factor. Also, as for the parasternal intercostals, the internal interosseous intercostal muscles in the dog are known to be insensitive to vibration, in particular when vibration is delivered during the inspiratory phase of the breathing cycle (Leduc et al. 2001). Consequently, even though these muscles were not recorded in this study, it is highly improbable that they played any significant role either. The conclusion can be drawn, therefore, that during ribcage vibration, stretch reflexes in external intercostal muscles generate only small tension.
The animals of this study, however, were anaesthetized with barbiturates, and substantial evidence has been produced that in such animals, the inspiratory elevation of the ribs during resting breathing results partly from the action of the external intercostals but predominantly from the action of the parasternal intercostals (De Troyer, 1991b; De Troyer & Wilson, 2000). Whether this feature is a species characteristic or the result of anaesthesia has not been assessed. However, since the increase in external intercostal activity during ribcage vibration was only 40-60 % relative to the activity recorded in the non-vibrated breaths, spindle-induced alterations in rib elevation might be difficult to demonstrate. On the other hand, it is well established that a sudden increase in inspiratory mechanical load in anaesthetized cats and dogs, operating through the large fall in pleural pressure, reverses the normal inspiratory shortening of the external intercostal muscles in the rostral segments of the ribcage into an inspiratory muscle lengthening (De Troyer, 1992) and thereby elicits a marked increase in afferent discharges from intercostal muscle spindles (Corda et al. 1965). As a result, there is an increase in the rate of rise of external intercostal activity, which is abolished after section of the appropriate dorsal roots (Corda et al. 1965; Sant'Ambrogio & Widdicombe, 1965; Shannon & Zechman, 1972; De Troyer, 1991a). And indeed, when the animals of this study were given high inspiratory airflow resistances or when the airway was occluded at end-expiration for a single breath, the external intercostals showed a clear-cut facilitation and peak inspiratory EMG activity increased, on average, by a factor of six (Fig. 3A-C). Yet, when the muscles in all interspaces were severed, the inspiratory axial displacement of the rib showed little or no change (Fig. 4). Thus, although the increase in external intercostal activity during loaded breaths was much larger than during ribcage vibration, the tension generated by the muscles still appeared to be small.
Before this conclusion can be drawn, however, a number of variables need to be considered. First, rib displacement in this study was measured along the craniocaudal axis of the ribcage, and it could be argued that sectioning the external intercostal muscles altered rib displacement along a different axis. In the dog, however, whereas the parasternal intercostals drive the ribs both cranially and outward, the external intercostals drive the ribs primarily in the cranial direction (De Troyer & Wilson, 2000). Consequently, if the external intercostals developed a significant tension during loaded breaths, it is unlikely that sectioning them would alter the lateral displacement of the ribs without also affecting their craniocaudal displacement. Second, sectioning the external intercostals might elicit a compensatory increase in parasternal intercostal inspiratory activity in the same way that denervation of the parasternal intercostals induces an increase in external intercostal activity (De Troyer & Yuehua, 1994); or alternatively, sectioning the external intercostals might cause a reduction in the fall in pleural pressure during loaded breaths. Either alteration would obscure any change in rib displacement that suppression of external intercostal muscle force might otherwise produce. Whatever the load, however, no change in parasternal intercostal EMG activity or in Ppl was seen after muscle section (Fig. 3D and Fig. 5).
The lack of significant alteration in rib displacement after section of the external intercostals could also relate to the elastic properties of the ribcage. Thus, studies by D'Angelo & Sant'Ambrogio (1974) have shown that the ribcage in dogs becomes less compliant when it contracts below its resting, end-expiratory volume. Since the ribs moved caudally during breathing against high inspiratory airflow resistances and during airway occlusion, the ribcage was therefore displaced to a stiffer portion of its pressure- volume curve. If the ribcage in these breaths were stiff enough, then sectioning the external intercostals might induce a significant reduction in the force applied to the ribs, but only a minimal increase in caudal rib displacement. Denervation of the parasternal intercostals was performed to evaluate the potential importance of this mechanism. The fall in pleural pressure after denervation was diminished (Fig. 5), yet the inspiratory caudal displacement of the ribs was substantially augmented (Fig. 4). The conclusion clearly emerges, therefore, that the lack of alteration in rib displacement after section of the external intercostals cannot be accounted for on the basis of the elastic properties of the ribcage, and hence, that the force generated by these muscles during loaded breaths is indeed small. As a corollary, since the inspiratory EMG activity recorded from the muscles during such breaths reflects the net input provided to the motoneurone pool by central respiratory drive potentials, afferents from muscle spindles and afferents from rib joint receptors (Sears, 1964; De Troyer, 1996), the tension resulting from intercostal stretch reflexes must be even smaller.
Facilitation of external intercostal activity during mechanical loading has traditionally been envisaged as representing the operation of a 'length follow-up servo mechanism' (Critchlow & von Euler, 1963; Sears, 1964). That is, an increased opposition to inspiration would cause the external intercostal muscles to shorten at a slower rate, leading to a misalignment between the intrafusal fibres and the extrafusal muscle fibres. The resulting increase in spindle afferent input would then elicit excitatory post-synaptic potentials (EPSPs) in the corresponding 
-motoneurones, such that the force of contraction of the extrafusal fibres would be enhanced and muscle shortening (and, with it, rib cranial displacement) would be restored. More recently, however, the efficiency of this feedback system was questioned (De Troyer, 1992), and the current findings provide strong evidence that in lightly anaesthetized animals, this control mechanism is indeed ineffective in modifying the mechanical behaviour of the respiratory system. In agreement with several observations on limb muscles (Tardieu et al. 1968; Matthews & Stein, 1969; Vallbo 1974; Pierrot-Deseilligny & Mazières, 1984), these findings thus support the concept that instead, intercostal muscle spindles would primarily allow the central nervous system to monitor progress of the movements related to breathing and to adjust for minimal disturbances. These muscle spindles might play a similar role in non-respiratory movements, particularly during rotations of the trunk (Decramer et al. 1986; Whitelaw et al. 1992).
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Acknowledgements
This work was supported by a research grant from the Brussels School of Medicine.
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), after section of the external intercostal muscles (
), and after denervation of the parasternal intercostal muscles (
). Positive rib motions indicate inspiratory displacements in the cranial direction, and negative motions indicate inspiratory displacements in the caudal direction.