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Journal of Physiology (2001), 534.3, pp. 873-880
© Copyright 2001 The Physiological Society
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ABSTRACT |
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INTRODUCTION |
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It is well established that in the dog, the internal intercostal muscles of the parasternal region (the so-called parasternal intercostals) and the external intercostal muscles in the rostral interspaces contract during the inspiratory phase of the breathing cycle to produce elevation of the ribs and expansion of the rib cage (De Troyer, 1991; De Troyer & Wilson, 2000). Electromyographic studies in awake animals, however, have recently emphasized a difference in the pattern of activity between these two sets of muscles (Easton et al. 1999). Specifically, activity in the parasternal intercostal muscles terminates with or near the cessation of inspiratory airflow, whereas activity in the rostral external intercostal muscles commonly persists well after the end of inspiratory airflow. To the extent that the external intercostals are more abundantly supplied with muscle spindles than the parasternal intercostals (Duron et al. 1978), the suggestion was made that the greater post-inspiratory activity in these muscles could be related to a spindle mechanism (Easton et al. 1999).
The operation of muscle spindles in the occurrence of post-inspiratory activity could be envisaged as follows. After peak inspiration, as the ribs move caudally back towards their relaxation position, the external intercostal muscles in the rostral interspaces and the parasternal intercostal muscles lengthen rather abruptly (De Troyer, 1992; Di Marco et al. 1992). Therefore, the central, sensitive portion of the spindles in both muscles should be stretched. Since the external intercostal muscles contain large numbers of spindles, the corresponding 
-motoneurones could receive many excitatory post-synaptic potentials (EPSPs), and so they might be maintained above activation threshold in early expiration. As a result, efferent -motor activity to the muscles would be prolonged. On the other hand, as the parasternal intercostals are poorly endowed with muscle spindles, the number of unitary EPSPs reaching the -motoneurones in early expiration should be smaller such that these motoneurones would repolarize more rapidly.
The electrical recordings from thoracic dorsal roots made by Critchlow & von Euler (1963) in spontaneously breathing cats did not show any increase in afferent activity from external intercostal muscle spindles in early expiration. Afferent activity was actually found to be stable throughout expiration or to decrease temporarily in the early post-inspiratory period. However, these recordings were obtained from mid-thoracic segments (T5-T7), and measurements of the respiratory changes in intercostal muscle length in dogs (Decramer et al. 1986) and in cats (Greer & Stein, 1989) have demonstrated that in contrast to the rostral segments, the external intercostal muscles in the mid-thoracic segments do commonly lengthen during inspiration and shorten in early expiration. The segments studied by Critchlow & von Euler (1963) also increased markedly in width during inspiration, thus suggesting that the muscle fibres connecting the two ribs, including those of the external intercostal, were similarly lengthening during inspiration. Moreover, in that study, recordings from external intercostal spindle afferents were also obtained during electrical stimulation of the ventral roots with single shocks. Each shock led to a clear-cut narrowing of the segment together with a suppression of spindle afferent discharges, but during the subsequent relaxation phase, at the time when the segment was widening and the muscle presumably was lengthening, there was a definite, transient increase in spindle afferent discharges (see Plates 1(i)B and 2A and B in Critchlow & von Euler, 1963). This implies that if the external intercostal muscles lengthened sufficiently in the early post-inspiratory period, an increase in spindle afferent discharges might also occur. In fact, however, nothing is known of the role played by muscle spindles in determining post-inspiratory activity in the intercostal muscles, and the present studies were designed to elucidate it.
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METHODS |
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The experiments were performed on adult mongrel dogs (14-36 kg) anaesthetized with pentobarbital sodium (initial dose, 25 mg kg-1 I.V.), as approved by the Animal Ethics and Welfare Committee of the Brussels School of Medicine. The animals were placed in the supine posture and intubated with a cuffed endotracheal tube, and a venous cannula was inserted in the forelimb to give maintenance doses of anaesthetic. A catheter was also inserted in the femoral artery to monitor blood pressure and sample arterial blood periodically for blood gas analysis, after which the rib cage and intercostal muscles were exposed on the right side of the chest from the first to the eighth rib by deflection of the skin and underlying muscle layers. The vagi were finally isolated bilaterally in the neck, infiltrated with 2 % lidocaine (lignocaine) and sectioned.
The measurements were essentially similar to those described in a previous investigation (De Troyer, 1996). Airflow at the endotracheal tube was measured with a heated Fleisch pneumotachograph connected to a differential pressure transducer (Validyne, Northridge, CA, USA), and lung volume was obtained by electronic integration of the flow signal. Electromyographic (EMG) activity was recorded from the parasternal intercostal and external intercostal muscles in the second interspace with pairs of silver hook electrodes spaced 3-4 mm apart. Each 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 (Kirkwood et al. 1982; Greer & Martin, 1990; Legrand & De Troyer, 1999). The two 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. In addition, the craniocaudal (axial) displacement of the third rib was measured with a linear displacement transducer (Schaevitz Eng. Pennsauken, NJ, USA), and the changes in external intercostal 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). It should be pointed out, however, that the piezoelectric crystals were placed within 10 mm of the EMG electrodes; electrical activity and changes in muscle length, therefore, were recorded from the same portion of the muscle.
The animals were allowed to recover for 30 min after instrumentation, after which measurements of airflow, lung volume, EMG activity, rib motion and muscle length during spontaneous room air breathing were made. Several animals did not have any post-inspiratory EMG activity in the external and parasternal intercostal muscles, even after strong pinching of the skin and repeated passive movements of the forelimbs (Sears, 1964); they were, therefore, included in another study. Ten animals, however, showed post-inspiratory activity with every breath, and in each of them, we manipulated the displacements of the ribs in early expiration so as to alter the changes in muscle length. A hook equipped with a small string was thus implanted into the third rib about 1 cm ventral to the piezoelectric crystals, and every 5-10 breaths, the axial displacement of the rib was altered manually for a single breath. The investigator received continuous feedback of parasternal intercostal EMG activity (via a loudspeaker) and external intercostal length (via a storage oscilloscope) so that the manipulation could be initiated immediately after the end of inspiration. Two series of manipulations were performed. In the first one, the rib was pulled caudally to increase the velocity of the caudal rib displacement and of the muscle lengthening in early expiration. In the second one, the rib was pulled cranially and maintained at or near its end-inspiratory position, such that the normal lengthening of the muscles was reduced or abolished. At least 10 trials of caudal and cranial rib manipulation were performed in each animal. Several trials were also performed in which the rib was manipulated abruptly after the post-inspiratory EMG activity had begun.
An additional procedure was performed in four animals to assess the respective roles of the changes in muscle length and of the changes in rib motion in inducing the alterations in post-inspiratory activity during rib manipulation. Thus, after completion of the control procedure, two clamps were attached firmly to the second and third ribs at resting end-expiration, such that the displacement of the ribs could be manipulated without affecting muscle length. One clamp was placed in the ventral part of the ribs, 1 cm dorsal to the chondrocostal junctions, and the other was placed dorsally in the rib angles. In addition, the external intercostal muscles in interspaces 1, 3 and 4 were sectioned midway between their rostral and caudal insertions from the costochondral junction to the rib angle, after which the cranial manipulation of the third rib was repeated. The two clamps were finally removed, and a last set of cranial rib manipulation was performed.
The animals were maintained under light surgical anaesthesia throughout the measurements. Supplementary doses of anaesthetic (1-2 mg kg-1) were given at regular intervals to ensure that there was no spontaneous movement of the fore- or hindlimbs, no flexor withdrawal of the forelimbs, and no pupillary light reflex. No alteration in blood pressure occurred either, including during manipulation of the ribs. The corneal reflex, however, was retained, and rectal temperature was maintained between 36 and 38 °C with infrared lamps. At the end of the experiment, the animal was given an overdose of anaesthetic (30-40 mg kg-1 I.V.).
Data analysis
As anticipated, the third rib in all animals moved cranially during inspiration and caudally during expiration. Concomitantly, the external intercostal muscle in the second interspace shortened gradually during inspiration, reached its shortest length at peak inspiration, and then lengthened toward its resting length (Lr) in early expiration. In each animal, this increase in muscle length was expressed as a percentage change relative to Lr, and the mechanical effect of rib manipulation was quantified by comparing the rate of muscle lengthening (expressed as % Lr s-1) recorded during each manipulated breath to that observed during the immediately preceding non-manipulated (control) breath.
The effect of rib manipulation on post-inspiratory EMG activity was quantified in two ways. First, the timing of inspiration was determined from the airflow tracing, and the termination of parasternal intercostal and external intercostal activity for each manipulated breath and the preceding control breath was measured relative to the ending of inspiratory airflow. This measurement was made on the basis of the raw EMG signals; the values thus obtained, therefore, were not corrupted by the time constant of the integrators. To allow comparison between the different animals, these values were expressed as percentages of expiratory time (TE). Second, the amount of post-inspiratory activity in each manipulated breath and each control breath was assessed by measuring the peak height of the integrated EMG signal in arbitrary units (a.u.).
Measurements of post-inspiratory EMG activity and rate of muscle lengthening were averaged over all trials in each individual animal, and they were then averaged for the animal group; these data are presented as means ± S.E.M. Statistical assessments of the effects of caudal and cranial rib manipulation on these variables and statistical comparison between the duration of post-inspiratory EMG activity in the parasternal intercostal and external intercostal muscles during the control breaths were made using Student's paired t tests. The criterion for statistical significance was taken as P < 0.05.
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RESULTS |
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Baseline data
The 10 animals of the study had a mean arterial PCO2 of 39.4 ± 1.2 mmHg and a mean arterial PO2 of 78.3 ± 2.9 mmHg; representative records of parasternal intercostal and external intercostal EMG activity during resting, unmanipulated breathing are shown in Fig. 1. All animals had post-inspiratory activity in the external intercostal muscle, whereas only six had post-inspiratory activity in the parasternal intercostal muscle. In addition, whenever post-inspiratory activity was recorded from both muscles, its duration was much longer in the external than in the parasternal intercostal muscle; a breath with longer parasternal post-inspiratory activity was not seen in any animal. For the animal group, therefore, whereas post-inspiratory activity in the external intercostal muscle lasted for 22.3 ± 5.8 % TE, post-inspiratory activity in the parasternal intercostal muscle lasted for only 1.6 ± 0.7 % TE (P = 0.001).
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Figure 1. Pattern of EMG activity in the parasternal and external intercostal muscles during resting breathing Traces were obtained in a representative animal. The two muscles were electrically active during the inspiratory phase of the breathing cycle. However, whereas activity in the parasternal intercostal muscle terminated shortly after the cessation of inspiratory airflow (vertical dotted line), activity in the external intercostal muscle persisted well after the end of inspiratory airflow. This post-inspiratory EMG activity occurs while the ribs are displaced caudally (downward deflection) and the muscle lengthens towards its resting length (Lr). | ||
Effects of rib manipulation
Manipulating the displacement of the rib in early expiration elicited significant changes in the post-inspiratory EMG activity recorded from the external intercostal muscle, as shown in Fig. 2 and Fig. 3. When the rib was pulled in the caudal direction, so that the rate of external intercostal muscle lengthening was increased from 48.9 ± 5.5 to 88.2 ± 10.1 % Lr s-1 (P < 0.001), post-inspiratory activity in the muscle was consistently enhanced (Fig. 2). For the 10 animals studied, the peak height of the integrated EMG signal was thus increased from 7.2 ± 0.8 to 13.4 ± 1.2 a.u. (P < 0.001). Conversely, when the rib was pulled in the cranial direction and maintained near its end-inspiratory position (Fig. 3), the rate of muscle lengthening was reduced from 46.0 ± 5.9 to 2.7 ± 0.5 % Lr s-1 (P < 0.001) and the peak height of post-inspiratory EMG activity was reduced from 9.8 ± 1.1 to 2.6 ± 0.5 a.u. (P < 0.001). With a cranial pull on the rib, the duration of external intercostal post-inspiratory activity was also markedly reduced from 22.8 ± 6.0 to 6.3 ± 2.2 % TE (P = 0.01). In contrast, whether the rib was pulled caudally or cranially, post-inspiratory EMG activity in the parasternal intercostal muscle remained unchanged.
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Figure 2. Response of the external intercostal muscle to caudal rib displacement in early expiration Traces were obtained in a representative animal. In the second breath shown, the third rib was pulled caudally after the end of inspiration (arrow) so that the rate of muscle lengthening was increased. This resulted in a marked increase in the post-inspiratory activity recorded from the external intercostal muscle, but post-inspiratory activity in the parasternal intercostal muscle remained unchanged. | ||
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Figure 3. Response of the external intercostal muscle to cranial rib displacement in early expiration Traces were obtained from the same animal as in Fig. 1. In the second breath, the third rib was pulled cranially after the end of inspiration (arrow) so that the normal muscle lengthening was essentially abolished. Concomitantly, the post-inspiratory activity recorded from the external intercostal muscle was reduced in amplitude and in duration. | ||
Abrupt changes in the pattern of rib motion in the early post-inspiratory period also caused marked alterations in the pattern of external intercostal post-inspiratory EMG activity without affecting parasternal activity. When the rib was pulled abruptly in the caudal direction, leading to a transient increase in the rate of muscle lengthening, the external intercostal post-inspiratory activity showed an immediate facilitation. In contrast, when the rib was pulled abruptly in the cranial direction, so that the normal muscle lengthening was reversed into a muscle shortening, the external intercostal post-inspiratory activity showed an immediate clear-cut reduction. In most trials, post-inspiratory activity was, in fact, temporarily suppressed (Fig. 4).
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Figure 4. Changes in intercostal post-inspiratory activities during abrupt cranial rib displacement Traces were obtained during a control breath and a manipulated breath (arrows) in a representative animal. When the rib was pulled cranially (first vertical line) in the post-inspiratory period, the normal muscle lengthening was temporarily reversed into a muscle shortening and this was associated with an immediate suppression of post-inspiratory activity in the external intercostal muscle. This activity re-appeared immediately after the pull was released (second vertical line). | ||
Effects of rib clamping
The effects of rib clamping on external intercostal post-inspiratory EMG activity in the four animals studied are summarized in Fig. 5. When the second and third ribs were attached together, so that the external intercostal muscle essentially remained constant in length, post-inspiratory activity during control, unmanipulated breathing decreased in amplitude in each animal (P < 0.001; Fig. 5A and B). In addition, whereas post-inspiratory activity before clamping was markedly decreased in response to cranial rib manipulation in early expiration (Fig. 5A), after clamping, no change occurred (Fig. 5B). On the other hand, when the clamps were removed, a definite post-inspiratory activity re-appeared in all animals during control breathing, and the inhibitory effect of cranial rib manipulation on this activity was re-established (Fig. 5C).
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Figure 5. Effects of rib clamping on external intercostal post-inspiratory activity Data were obtained in four animals before (A) and after (B) clamping the two ribs making up the intercostal space. In each panel, each pair of bars corresponds to the mean ± S.E.M. values (expressed as arbitrary units, a.u.) obtained during control, unmanipulated breathing ( | ||
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DISCUSSION |
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If muscle spindles played a major role in the occurrence of post-inspiratory EMG activity in the rostral external intercostal muscles, one would expect that reducing or suppressing the lengthening of the muscles in early expiration would elicit, through a decrease in spindle afferent discharges, a reduction in activity. Conversely, increasing the rate of muscle lengthening would increase the spindle afferent discharges and accentuate post-inspiratory activity. As shown in Figs 2-4, this is exactly what we observed. In every animal, post-inspiratory EMG activity in the external intercostal muscles showed a reflex decrease whenever the normal muscle lengthening in early expiration was suppressed or reversed into a muscle shortening, and it showed a reflex increase whenever the rate of muscle lengthening was augmented. As the animals had bilateral cervical vagotomy, these reflex responses cannot be related to alterations in vagal afferent inputs from the lungs. These responses, therefore, are fully consistent with our hypothesis that post-inspiratory activity in the rostral external intercostal muscles primarily represents the operation of a spinal stretch reflex.
The changes in external intercostal muscle length induced in our animals, however, were produced by altering the normal caudal displacement of the ribs, and recordings of afferent discharges from mechanoreceptors in the costovertebral joints of rabbits and cats have shown that these receptors also respond to rib displacement (Godwin-Austen, 1969). In fact, a large majority of them decrease their discharge rates when the ribs are displaced in the cranial direction and increase their discharge rates when the ribs are displaced in the caudal direction. Such variations in afferent activity were already recorded during quiet, resting breathing, thus indicating that the threshold of activity of these joint receptors is relatively low. In addition, strong evidence has recently been provided suggesting that in the dog, these receptors may modulate the EMG activity recorded from the external intercostal muscles during inspiration, increasing it when the ribs are displaced caudally and decreasing it when the ribs are displaced cranially (De Troyer, 1996, 1997). Therefore, to the extent that muscle lengthening in our animals was decreased through a reduction in the caudal displacement of the ribs, the possibility existed that the decreased post-inspiratory activity in the external intercostal muscles resulted from the suppression of afferent inputs from joint receptors, rather than muscle spindles. Similarly, as the rate of muscle lengthening was increased through a caudal displacement of the ribs, the observed increase in post-inspiratory activity might be primarily related to increased afferent inputs from joint receptors.
The potential role of these receptors was tested by locking together the two ribs making up the interspace investigated. Furthermore, because previous recordings from respiratory motoneurones in the thoracic spinal cord in cats have established that the spindles situated in a given external intercostal muscle project not only to the -motoneurones of this muscle but also to the external intercostal -motoneurones in adjacent segments (Eccles et al. 1963; Kirkwood & Sears, 1982b), the external intercostal muscles in the rostral interspace and in the two caudal interspaces were severed. Consequently, muscle length was kept constant and most intersegmental spindle reflexes were eliminated, thus leaving the joint reflexes virtually alone. Post-inspiratory EMG activity in the external intercostal muscles was found to be markedly reduced in this condition (Fig. 5). More importantly, no further decrease in post-inspiratory activity was seen when the ribs were maintained cranially in early expiration. Conversely, when the ribs were unlocked to re-establish normal respiratory changes in muscle length, a definite post-inspiratory activity reappeared during resting, unmanipulated breathing and the inhibitory effect of cranial rib manipulation was restored. The conclusion must be drawn, therefore, that reflexes from muscle spindles, but not rib joint receptors, are indeed a primary determinant of post-inspiratory EMG activity in the rostral external intercostal muscles. As a corollary, the control of external intercostal motoneurones by their reflex inputs in post-inspiration would be different from that during inspiration, at which time inputs from joint receptors actually appear to have a larger influence on external intercostal activity than inputs from muscle spindles (De Troyer, 1996, 1997). Studies in cats by Kirkwood & Sears (1982a), however, have indicated that the size of EPSPs induced in external intercostal motoneurones by primary spindle afferents is greater during inspiration than during expiration. Therefore, even though these investigators did not specifically investigate the early post-inspiratory period, the speculation must be offered that inputs from joint receptors are gated by the respiratory cycle, i.e. reach the external intercostal motoneurones only during inspiration.
We do not mean to imply that post-inspiratory EMG activity in the rostral external intercostal muscles is entirely due to muscle spindle afferents. In view of the usual inhibitory effect of Golgi tendon organ afferents on homonymous and synergic motoneurones (Jami, 1992) and of the rapid decrease in tension that must occur in the muscles after the end of inspiration, these afferents would be expected to play little or no role in this phenomenon. On the other hand, most animals in this study still had a small post-inspiratory activity when the ribs were maintained cranially after peak inspiration. Also, three of four animals had residual post-inspiratory activity in the external intercostal muscles after the ribs were locked and the muscles in adjacent segments were severed (Fig. 5). These findings suggest that this activity is also determined by central mechanisms, and indeed, intracellular recordings from medullary inspiratory neurones in cats have shown that neurones with a peak discharge frequency in late inspiration continue to discharge in early expiration. Neurones with a peak discharge frequency in early expiration have also been identified (Richter, 1982; Bianchi et al. 1995). In the case of the parasternal intercostal muscles, whose post-inspiratory EMG activity remained unaltered in response to cranial and caudal rib manipulation, central mechanisms would appear to be the main, if not the only, determinant.
Although the post-inspiratory activities recorded from the external and parasternal intercostal muscles during unmanipulated breathing had a similar duration to those observed in awake animals by Easton et al. (1999), post-inspiratory activity in the rostral external intercostal muscles appeared to be a more consistent finding in those animals. It has long been established that increasing the depth of anaesthesia by further injections of barbiturates in cats may rapidly reduce efferent activity from external intercostal - and fusimotor neurones (Sears, 1964). More recently, Di Marco et al. (1994) have also shown in dogs that inspiratory EMG activity in the rostral external intercostal muscles is more sensitive to anaesthesia than the inspiratory activities recorded from the diaphragm and parasternal intercostal muscles. Thus, in the presence of barbiturate anaesthesia, the external intercostal -motoneurones have a higher activation threshold or depolarize less during inspiration, so EPSPs from homonymous muscle spindles may be insufficient to induce persistent -motoneurone activity after the cessation of inspiratory airflow. On this basis, the absence of post-inspiratory EMG activity in several animals of this study may be understood, yet the argument could be made then that the current observations are not representative of the mechanisms controlling this activity in the absence of anaesthesia. That is, the contribution of medullary neurones to external intercostal post-inspiratory EMG activity in awake animals could be greater than that of spindle reflexes. We have no data to exclude this possibility, but the large difference observed in such animals between the parasternal intercostals and the external intercostals (Easton et al. 1999) argues against it. Late inspiratory and post-inspiratory neurones in the medulla are likely indeed to govern equally these two sets of motoneurones.
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Acknowledgements
This work was supported in part by the National Heart, Lung, and Blood Institute (USA) (grant HL-45 545).
Corresponding author
A. De Troyer: Chest Service, Erasme University Hospital, 808 Route de Lennik, 1070 Brussels, Belgium.
Author's present address
S. V. Berdah: Service de Chirurgie digestive, Hopital Nord, Chemin des Bourrely, 13915 Marseille, France.
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) and during cranial rib displacement after peak inspiration (
). Asterisks indicate statistically significant (P < 0.001) reductions in post-inspiratory activity during rib manipulation. After clamping, the post-inspiratory activity recorded from the external intercostal muscle was reduced and no longer decreased in response to cranial rib manipulation. The data shown in C were obtained after removal of the rib clamps and were similar to those before clamping.