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Mechanical Properties of Airway Smooth Muscle

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Abstract

The sections in this article are:

1 Airway Smooth Muscle
1.1 Length‐Tension Relationships
1.2 Force‐Velocity Relationships
1.3 Stimulus‐Response Relationships
1.4 Myogenic Responses
1.5 Contractility
1.6 Series‐Elastic Component
1.7 Maximum Force Potential (Active State)
1.8 Relaxation
1.9 Length Forcing
1.10 Heterogeneity of Mechanical Properties
1.11 Mechanics of Lung Strips
2 Contractile Interstitial Cells of the Lung
3 Functional Role of Airway Smooth Muscle
4 Conclusion
Figure 1. Figure 1.

Mean length‐tension curves of canine tracheal smooth muscle. “Resting tension” curve is obtained after using pharmacological relaxants or by inhibiting energy‐producing metabolic processes to preclude any spontaneous resting tone. The shape of this curve is typical of noncontractile biological tissues and results primarily from presence of elastin and collagen. With activation at a given length, tension rises to a level shown by the “total tension” curve. Difference in tension between total and resting curves represents activity of contractile element or force generator of muscle and is replotted as “active tension.” It is maximum at a unique length, which is arbitrarily defined as lo (lmax). Note: full curve not shown. Bars indicate standard errors.

Adapted from Stephens et al. 55
Figure 2. Figure 2.

Mean length‐total tension curves elicited in different ways for the tracheal smooth muscle preparations. Curve 4 is the conventional isometric tetanic length‐tension curve, as in Fig. 1. Curve 3 was obtained from experiments in which the muscle first shortened isotonically from lo (carrying the preload needed to set it at that length) and then contracted isometrically at a preselected length. Curve 2 was obtained from conventional afterloaded contractions in which the muscle first contracted isometrically at lo and then shortened isotonically. Curve 1 was obtained from freeloaded contractions, in which the muscle was first loaded (and allowed to lengthen in response to the load) before being (isotonically) contracted from the loaded length.

Adapted from Stephens and Van Niekerk 59
Figure 3. Figure 3.

Mean length‐tension curves for tracheal smooth muscle. Ca2+ concentration for upper curve is 4.75 mM and for lower curve is 2.0 mM. Bars indicate standard errors.

Adapted from Stephens et al. 58
Figure 4. Figure 4.

Data of Fig. 3 shown in normalized units.

Adapted from Stephens et al. 58
Figure 5. Figure 5.

Mean force‐velocity curve of tracheal smooth muscle. All experiments conducted at lo (lmax). Bars indicate standard errors.

Adapted from Stephens et al. 55
Figure 6. Figure 6.

Mean force‐velocity curves elicited during shortening and elongation of activated tracheal smooth muscle. Broken curve is extrapolated.

Adapted from Hanks and Stephens 19
Figure 7. Figure 7.

Mean stimulus‐response curve for tracheal smooth muscle. Tension is expressed as percent of Po. Bars indicate standard errors.

Adapted from Stephens 51
Figure 8. Figure 8.

Bottom: active isometric tension records (for typical tracheal smooth muscle) as functions of time. Calibration represents 4 g vertically and 2 s horizontally. Curves from top to bottom represent tension records obtained with muscle lengths set at lo, 0.8 lo, 0.6 lo, and 0.4 lo. Top: curves represent dP/dt values (P, active tension; t, time) obtained by electrical differentiation of bottom curves. Calibration represents 0.5 g · s−1 vertically and 2 s horizontally.

Adapted from Stephens and Kroeger 53
Figure 9. Figure 9.

Active isometric tension traces from spontaneously contracting tracheal smooth muscle. Left panel shows absence of a myogenic response before treatment with tetraethylammonium chloride. Right panel shows presence of a myogenic response after tetraethylammonium chloride treatment. Middle panel shows phasic activity of 2 periodicities.

Adapted from Stephens et al. 54
Figure 10. Figure 10.

Velocity‐length phase planes of three contractions elicited from canine tracheal smooth muscle. Curve 1, plane with 8‐mN load imposed on muscle; curve 2, plane with 28‐mN load. In dashed line 3a, load was abruptly changed from 8 to 28 mN at midpoint of shortening, then back to 8 mN near end of shortening. In dashed line 3b, load clamped from 8 to 28 mN early in shortening, then changed back to 8 mN at 0.7 lo. In dashed line 3c, load again changed from 8 mN to 28 mN early, then at ∼0.5 lo changed back to 8 mN.

Figure 11. Figure 11.

Time course of maximal force potentials (P′o) in tetanic isotonic contractions of tracheal smooth muscles. Mean values of force development in control isometric contractions (Po) and force potential (P′o) measured in isotonic contractions are shown. P′o values obtained from highest possible force level, i.e., where clamped load could be sustained for 100 ms, for load clamps at various times during time course of isotonic tetanic contraction. Po values obtained from corresponding isotonic control contractions. Bars indicate standard errors.

Figure 12. Figure 12.

Two larger panels at left show length (upper) and force (lower) traces of a series of afterloaded isotonic contractions. Inset panels at right show contractions with different afterloads up to a full isometric tetanus in cat heart papillary muscle (A) and frog ventricular muscle (B).

Figure 13. Figure 13.

Length‐tension plots in 2 dog trachealis muscle strips. Total range of lengths in sequence is approximately that undergone by trachealis in a vital capacity maneuver. When relaxed with isoproterenol and atropine, tensions were low. Tension in contracted strip is primarily due to active component. When carbachol was added to the bath, with strip held at constant length, tension increased over 1 min to ∼10 g. A: muscle was then lengthened from 37 mm to 42 mm, cycled twice over ∼0.5 mm, lengthened to 44 mm, cycled twice over ∼0.5 mm, and lengthened to 45 mm. It was then shortened with similar pattern of interrupting small cycles. Entire sequence took ∼1 min. B: a muscle strip was cycled 5 times over 10% of its length. Each cycle compromised an 8‐s lengthening and either an 8‐s (continuous tracing) or a 4‐s (dashed tracing) shortening, followed by a pause lasting 0–5 min. During these pauses, force increased isometrically to as much as 20 g at 5 min. Initial slope during subsequent lengthening was lower after longer pauses and was almost indistinguishable from isometric tracings.

Adapted from Sasaki and Hoppin 43
Figure 14. Figure 14.

Behavior of a carbachol‐controlled trachealis muscle strip during length cycling at different frequencies.

Adapted from Sasaki and Hoppin 43


Figure 1.

Mean length‐tension curves of canine tracheal smooth muscle. “Resting tension” curve is obtained after using pharmacological relaxants or by inhibiting energy‐producing metabolic processes to preclude any spontaneous resting tone. The shape of this curve is typical of noncontractile biological tissues and results primarily from presence of elastin and collagen. With activation at a given length, tension rises to a level shown by the “total tension” curve. Difference in tension between total and resting curves represents activity of contractile element or force generator of muscle and is replotted as “active tension.” It is maximum at a unique length, which is arbitrarily defined as lo (lmax). Note: full curve not shown. Bars indicate standard errors.

Adapted from Stephens et al. 55


Figure 2.

Mean length‐total tension curves elicited in different ways for the tracheal smooth muscle preparations. Curve 4 is the conventional isometric tetanic length‐tension curve, as in Fig. 1. Curve 3 was obtained from experiments in which the muscle first shortened isotonically from lo (carrying the preload needed to set it at that length) and then contracted isometrically at a preselected length. Curve 2 was obtained from conventional afterloaded contractions in which the muscle first contracted isometrically at lo and then shortened isotonically. Curve 1 was obtained from freeloaded contractions, in which the muscle was first loaded (and allowed to lengthen in response to the load) before being (isotonically) contracted from the loaded length.

Adapted from Stephens and Van Niekerk 59


Figure 3.

Mean length‐tension curves for tracheal smooth muscle. Ca2+ concentration for upper curve is 4.75 mM and for lower curve is 2.0 mM. Bars indicate standard errors.

Adapted from Stephens et al. 58


Figure 4.

Data of Fig. 3 shown in normalized units.

Adapted from Stephens et al. 58


Figure 5.

Mean force‐velocity curve of tracheal smooth muscle. All experiments conducted at lo (lmax). Bars indicate standard errors.

Adapted from Stephens et al. 55


Figure 6.

Mean force‐velocity curves elicited during shortening and elongation of activated tracheal smooth muscle. Broken curve is extrapolated.

Adapted from Hanks and Stephens 19


Figure 7.

Mean stimulus‐response curve for tracheal smooth muscle. Tension is expressed as percent of Po. Bars indicate standard errors.

Adapted from Stephens 51


Figure 8.

Bottom: active isometric tension records (for typical tracheal smooth muscle) as functions of time. Calibration represents 4 g vertically and 2 s horizontally. Curves from top to bottom represent tension records obtained with muscle lengths set at lo, 0.8 lo, 0.6 lo, and 0.4 lo. Top: curves represent dP/dt values (P, active tension; t, time) obtained by electrical differentiation of bottom curves. Calibration represents 0.5 g · s−1 vertically and 2 s horizontally.

Adapted from Stephens and Kroeger 53


Figure 9.

Active isometric tension traces from spontaneously contracting tracheal smooth muscle. Left panel shows absence of a myogenic response before treatment with tetraethylammonium chloride. Right panel shows presence of a myogenic response after tetraethylammonium chloride treatment. Middle panel shows phasic activity of 2 periodicities.

Adapted from Stephens et al. 54


Figure 10.

Velocity‐length phase planes of three contractions elicited from canine tracheal smooth muscle. Curve 1, plane with 8‐mN load imposed on muscle; curve 2, plane with 28‐mN load. In dashed line 3a, load was abruptly changed from 8 to 28 mN at midpoint of shortening, then back to 8 mN near end of shortening. In dashed line 3b, load clamped from 8 to 28 mN early in shortening, then changed back to 8 mN at 0.7 lo. In dashed line 3c, load again changed from 8 mN to 28 mN early, then at ∼0.5 lo changed back to 8 mN.



Figure 11.

Time course of maximal force potentials (P′o) in tetanic isotonic contractions of tracheal smooth muscles. Mean values of force development in control isometric contractions (Po) and force potential (P′o) measured in isotonic contractions are shown. P′o values obtained from highest possible force level, i.e., where clamped load could be sustained for 100 ms, for load clamps at various times during time course of isotonic tetanic contraction. Po values obtained from corresponding isotonic control contractions. Bars indicate standard errors.



Figure 12.

Two larger panels at left show length (upper) and force (lower) traces of a series of afterloaded isotonic contractions. Inset panels at right show contractions with different afterloads up to a full isometric tetanus in cat heart papillary muscle (A) and frog ventricular muscle (B).



Figure 13.

Length‐tension plots in 2 dog trachealis muscle strips. Total range of lengths in sequence is approximately that undergone by trachealis in a vital capacity maneuver. When relaxed with isoproterenol and atropine, tensions were low. Tension in contracted strip is primarily due to active component. When carbachol was added to the bath, with strip held at constant length, tension increased over 1 min to ∼10 g. A: muscle was then lengthened from 37 mm to 42 mm, cycled twice over ∼0.5 mm, lengthened to 44 mm, cycled twice over ∼0.5 mm, and lengthened to 45 mm. It was then shortened with similar pattern of interrupting small cycles. Entire sequence took ∼1 min. B: a muscle strip was cycled 5 times over 10% of its length. Each cycle compromised an 8‐s lengthening and either an 8‐s (continuous tracing) or a 4‐s (dashed tracing) shortening, followed by a pause lasting 0–5 min. During these pauses, force increased isometrically to as much as 20 g at 5 min. Initial slope during subsequent lengthening was lower after longer pauses and was almost indistinguishable from isometric tracings.

Adapted from Sasaki and Hoppin 43


Figure 14.

Behavior of a carbachol‐controlled trachealis muscle strip during length cycling at different frequencies.

Adapted from Sasaki and Hoppin 43
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How to Cite

Newman L. Stephens, Frederic G. Hoppin. Mechanical Properties of Airway Smooth Muscle. Compr Physiol 2011, Supplement 12: Handbook of Physiology, The Respiratory System, Mechanics of Breathing: 263-276. First published in print 1986. doi: 10.1002/cphy.cp030317