Mechanical effect of muscle spindles in the canine external intercostal muscles

Abstract

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 approximately 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.

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 (L_r). 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.

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.

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). P_pl, pleural pressure.

Figure 5. Effect of increased inspiratory resistance on P_pl

Mean ±s.e.m. data from nine animals. Same conventions as in Fig. 4.

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 (•), 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.

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).