Adjustable passive length-tension curve in rabbit detrusor smooth muscle

2007 ◽  
Vol 102 (5) ◽  
pp. 1746-1755 ◽  
Author(s):  
John E. Speich ◽  
Christopher Dosier ◽  
Lindsey Borgsmiller ◽  
Kevin Quintero ◽  
Harry P. Koo ◽  
...  
Keyword(s):  
Smooth Muscle ◽  
Strain Softening ◽  
Muscle Length ◽  
Strain History ◽  
Total Force ◽  
Detrusor Smooth Muscle ◽  
Passive Force ◽  
Passive Stiffness ◽  
Active Force ◽  
Length Changes

Until the 1990s, the passive and active length-tension ( L-T) relationships of smooth muscle were believed to be static, with a single passive force value and a single maximum active force value for each muscle length. However, recent studies have demonstrated that the active L-T relationship in airway smooth muscle is dynamic and adapts to length changes over a period of time. Furthermore, our prior work showed that the passive L-T relationship in rabbit detrusor smooth muscle (DSM) is also dynamic and that in addition to viscoelastic behavior, DSM displays strain-softening behavior characterized by a loss of passive stiffness at shorter lengths following a stretch to a new longer length. This loss of passive stiffness appears to be irreversible when the muscle is not producing active force and during submaximal activation but is reversible on full muscle activation, which indicates that the stiffness component of passive force lost to strain softening is adjustable in DSM. The present study demonstrates that the passive L-T curve for DSM is not static and can shift along the length axis as a function of strain history and activation history. This study also demonstrates that adjustable passive stiffness (APS) can modulate total force (35% increase) for a given muscle length, while active force remains relatively unchanged (4% increase). This finding suggests that the structures responsible for APS act in parallel with the contractile apparatus, and the results are used to further justify the configuration of modeling elements within our previously proposed mechanical model for APS.

scholarly journals Adaptation of the length-active tension relationship in rabbit detrusor

2009 ◽  
Vol 297 (4) ◽  
pp. F1119-F1128 ◽  
Author(s):  
John E. Speich ◽  
Atheer M. Almasri ◽  
Hersch Bhatia ◽  
Adam P. Klausner ◽  
Paul H. Ratz
Keyword(s):  
Smooth Muscles ◽  
Muscle Length ◽  
Strain History ◽  
Detrusor Smooth Muscle ◽  
Active Tension ◽  
Passive Stiffness ◽  
Vascular Smooth Muscles ◽  
Length Changes ◽  
Adjustable Passive Stiffness ◽  
First Time

Studies have shown that the length-tension ( L-T) relationships in airway and vascular smooth muscles are dynamic and can adapt to length changes over a period of time. Our prior studies have shown that the passive L-T relationship in rabbit detrusor smooth muscle (DSM) is also dynamic and that DSM exhibits adjustable passive stiffness (APS) characterized by a passive L-T curve that can shift along the length axis as a function of strain history and activation history. The present study demonstrates that the active L-T curve for DSM is also dynamic and that the peak active tension produced at a particular muscle length is a function of both strain and activation history. More specifically, this study reveals that the active L-T relationship, or curve, does not have a unique peak tension value with a single ascending and descending limb, but instead reveals that multiple ascending and descending limbs can be exhibited in the same DSM strip. This study also demonstrates that for DSM strips not stretched far enough to reveal a descending limb, the peak active tension produced by a maximal KCl-induced contraction at a short, passively slack muscle length of 3 mm was reduced by 58.6 ± 4.1% ( n = 1 5) following stretches to and contractions at threefold the original muscle length, 9 mm. Moreover, five subsequent contractions at the short muscle length displayed increasingly greater tension; active tension produced by the sixth contraction was 91.5 ± 9.1% of that produced by the prestretch contraction at that length. Together, these findings indicate for the first time that DSM exhibits length adaptation, similar to vascular and airway smooth muscles. In addition, our findings demonstrate that preconditioning, APS and adaptation of the active L-T curve can each impact the maximum total tension observed at a particular DSM length.

Length vs. active force relationship in single isolated smooth muscle cells

1991 ◽  
Vol 260 (5) ◽  
pp. C1104-C1112 ◽  
Author(s):  
D. E. Harris ◽  
D. M. Warshaw
Keyword(s):  
Smooth Muscle ◽  
Elastic Modulus ◽  
Smooth Muscle Cells ◽  
Force Measurement ◽  
Muscle Length ◽  
Muscle Cells ◽  
Active Force ◽  
Length Changes ◽  
Cross Bridges ◽  
Force Relationship

The length vs. active force relationship (L-F) may provide information about changes in smooth muscle contractile protein interactions as muscle length changes. To characterize the L-F in single toad stomach smooth muscle cells, cells were attached to a force measurement system, electrically stimulated, and isometric force and elastic modulus (an estimate of the number of attached cross bridges) determined at different cell lengths. Cells generated maximum stress (Pmax = 152.5 mN/mm2) and elastic modulus (Eact = 0.68 x 10(4) mN/mm2) at their rest length (Lcell = 78.0 microns; distance between cell attachments). At shorter lengths, active force and elastic modulus declined proportionally with active force eliminated at 0.4 Lcell. Stretching the relaxed cells up to 1.4 Lcell shifted the subsequent L-F along the length axis by the amount of the stretch but did not change Pmax or the shape of the L-F. In activated cells, force was a function of cell length rather than of shortening history. We interpret these findings as evidence that 1) Lcell is close to the optimum length for force generation, 2) the decline in force at lengths less than Lcell results from a reduced number of attached cross bridges, and 3) stretching relaxed smooth muscle cells may not move the contractile units to new positions on their L-F.

scholarly journals The length dependence of muscle active force: considerations for parallel elastic properties

2005 ◽  
Vol 98 (5) ◽  
pp. 1666-1673 ◽  
Author(s):  
Brian R. MacIntosh ◽  
Meredith B. MacNaughton
Keyword(s):  
Muscle Length ◽  
Element Model ◽  
Medial Gastrocnemius ◽  
Elastic Component ◽  
Contractile Element ◽  
Total Force ◽  
Passive Force ◽  
Active Force ◽  
Fascicle Length ◽  
The Relationship

The purpose of this study was to choose between two popular models of skeletal muscle: one with the parallel elastic component in parallel with both the contractile element and the series elastic component ( model A), and the other in which it is in parallel with only the contractile element ( model B). Passive and total forces were obtained at a variety of muscle lengths for the medial gastrocnemius muscle in anesthetized rats. Passive force was measured before the contraction ( passive A) or was estimated for the fascicle length at which peak total force occurred ( passive B). Fascicle length was measured with sonomicrometry. Active force was calculated by subtracting passive ( A or B) force from peak total force at each fascicle or muscle length. Optimal length, that fascicle length at which active force is maximized, was 13.1 ± 1.2 mm when passive A was subtracted and 14.0 ± 1.1 mm with passive B ( P < 0.01). Furthermore, the relationship between double-pulse contraction force and length was broader when calculated with passive B than with passive A. When the muscle was held at a long length, passive force decreased due to stress relaxation. This was accompanied by no change in fascicle length at the peak of the contraction and only a small corresponding decrease in peak total force. There is no explanation for the apparent increase in active force that would be obtained when subtracting passive A from the peak total force. Therefore, to calculate active force, it is appropriate to subtract passive force measured at the fascicle length corresponding to the length at which peak total force occurs, rather than passive force measured at the length at which the contraction begins.

scholarly journals Reports of the length dependence of fatigue are greatly exaggerated

2006 ◽  
Vol 101 (1) ◽  
pp. 23-29 ◽  
Author(s):  
M. B. MacNaughton ◽  
B. R. MacIntosh
Keyword(s):  
Muscle Length ◽  
Repetitive Stimulation ◽  
Double Pulse ◽  
Medial Gastrocnemius ◽  
Passive Force ◽  
Active Force ◽  
Rightward Shift ◽  
Length Dependence ◽  
Force Depression ◽  
In Series

Relative force depression associated with muscle fatigue is reported to be greater when assessed at short vs. long muscle lengths. This appears to be due to a rightward shift in the force-length relationship. This rightward shift may be caused by stretch of in-series structures, making sarcomere lengths shorter at any given muscle length. Submaximal force-length relationships (twitch, double pulse, 50 Hz) were evaluated before and after repetitive contractions (50 Hz, 300 ms, 1/s) in an in situ preparation of the rat medial gastrocnemius muscle. In some experiments, fascicle lengths were measured with sonomicrometry. Before repetitive stimulation, fascicle lengths were 11.3 ± 0.8, 12.8 ± 0.9, and 14.4 ± 1.2 mm at lengths corresponding to −3.6, 0, and 3.6 mm where 0 is a reference length that corresponds with maximal active force for double-pulse stimulation. After repetitive stimulation, there was no change in fascicle lengths; these lengths were 11.4 ± 0.8, 12.6 ± 0.9, and 14.2 ± 1.2 mm. The length dependence of fatigue was, therefore, not due to a stretch of in-series structures. Interestingly, the rightward shift that was evident when active force was calculated in the traditional way (subtraction of the passive force measured before contraction) was not seen when active force was calculated by subtracting the passive force that was associated with the fascicle length reached at the peak of the contraction. This calculation is based on the assumption that passive force decreases as the fascicles shorten during a fixed-end contraction. This alternative calculation revealed similar postfatigue absolute active force depression at all lengths. In relative terms, a length dependence of fatigue was still evident, but this was greatly diminished compared with that observed when active force was calculated with the traditional method.

Tracheal smooth muscle mechanics in vivo

1990 ◽  
Vol 68 (1) ◽  
pp. 209-219 ◽  
Author(s):  
M. Okazawa ◽  
P. Pare ◽  
J. Road
Keyword(s):  
Smooth Muscle ◽  
Muscle Mechanics ◽  
Muscle Length ◽  
Base Line ◽  
Maximal Velocity ◽  
Velocity Of Shortening ◽  
Length Changes ◽  
Trachealis Muscle

We applied the technique of sonomicrometry to directly measure length changes of the trachealis muscle in vivo. Pairs of small 1-mm piezoelectric transducers were placed in parallel with the muscle fibers in the posterior tracheal wall in seven anesthetized dogs. Length changes were recorded during mechanical ventilation and during complete pressure-volume curves of the lung. The trachealis muscle showed spontaneous fluctuations in base-line length that disappeared after vagotomy. Before vagotomy passive pressure-length curves showed marked hysteresis and length changed by 18.5 +/- 13.2% (SD) resting length at functional residual capacity (LFRC) from FRC to total lung capacity (TLC) and by 28.2 +/- 16.2% LFRC from FRC to residual volume (RV). After vagotomy hysteresis decreased considerably and length now changed by 10.4 +/- 3.7% LFRC from FRC to TLC and by 32.5 +/- 14.6% LFRC from FRC to RV. Bilateral supramaximal vagal stimulation produced a mean maximal active shortening of 28.8 +/- 14.2% resting length at any lung volume (LR) and shortening decreased at lengths above FRC. The mean maximal velocity of shortening was 4.2 +/- 3.9% LR.S-1. We conclude that sonomicrometry may be used to record smooth muscle length in vivo. Vagal tone strongly influences passive length change. In vivo active shortening and velocity of shortening are less than in vitro, implying that there are significant loads impeding shortening in vivo.

A mechanical model for adjustable passive stiffness in rabbit detrusor

2006 ◽  
Vol 101 (4) ◽  
pp. 1189-1198 ◽  
Author(s):  
John E. Speich ◽  
Kevin Quintero ◽  
Christopher Dosier ◽  
Lindsey Borgsmiller ◽  
Harry P. Koo ◽  
...  
Keyword(s):  
Steady State ◽  
Mechanical Model ◽  
Strain Softening ◽  
Slow Component ◽  
Viscoelastic Model ◽  
Passive Force ◽  
Passive Stiffness ◽  
Cross Link ◽  
Force Relaxation ◽  
Adjustable Passive Stiffness

Strips of rabbit detrusor smooth muscle (DSM) exhibit adjustable passive stiffness characterized by strain softening: a loss of stiffness on stretch to a new length distinct from viscoelastic behavior. At the molecular level, strain softening appears to be caused by cross-link breakage and is essentially irreversible when DSM is maintained under passive conditions (i.e., when cross bridges are not cycling to produce active force). However, on DSM activation, strain softening is reversible and likely due to cross-link reformation. Thus DSM displays adjustable passive stiffness that is dependent on the history of both muscle strain and activation. The present study provides empirical data showing that, in DSM, 1) passive isometric force relaxation includes a very slow component requiring hours to approach steady state, 2) the level of passive force maintained at steady state is less if the tissue has previously been strain softened, and 3) tissues subjected to a quick-release protocol exhibit a biphasic response consisting of passive force redevelopment followed by force relaxation. To explain these and previously identified characteristics, a mechanical model for adjustable passive stiffness is proposed based on the addition of a novel cross-linking element to a hybrid Kelvin/Voigt viscoelastic model.

scholarly journals Modeling the impairment of airway smooth muscle force by stretch

2015 ◽  
Vol 118 (6) ◽  
pp. 684-691 ◽  
Author(s):  
Jason H. T. Bates
Keyword(s):  
Smooth Muscle ◽  
Airway Smooth Muscle ◽  
Coarse Grained ◽  
Active Force ◽  
Cross Bridge ◽  
Bulk Force ◽  
Length Changes ◽  
Cross Bridges ◽  
Large Stretch ◽  
Two State Model

Imposed length changes of only a small percent produce transient reductions in active force in strips of airway smooth muscle (ASM) due to the temporary detachment of bound cross-bridges caused by the relative motion of the actin and myosin fibers. More dramatic and sustained reductions in active force occur following large changes in length. The Huxley two-state model of skeletal muscle originally proposed in 1957 and later adapted to include a four-state description of cross-bridge kinetics has been widely used to model the former phenomenon, but is unable to account for the latter unless modified to include mechanisms by which the contractile machinery in the ASM cell becomes appropriately rearranged. Even so, the Huxley model itself is based on the assumption that the contractile proteins are all aligned precisely in the direction of bulk force generation, which is not true for ASM. The present study derives a coarse-grained version of the Huxley model that is free of inherent assumptions about cross-bridge orientation. This simplified model recapitulates the key features observed in the force-length behavior of activated strips of ASM and, in addition, provides a mechanistically based way of accounting for the sustained force reductions that occur following large stretch.

ROK-induced cross-link formation stiffens passive muscle: reversible strain-induced stress softening in rabbit detrusor

2005 ◽  
Vol 289 (1) ◽  
pp. C12-C21 ◽  
Author(s):  
John E. Speich ◽  
Lindsey Borgsmiller ◽  
Chris Call ◽  
Ryan Mohr ◽  
Paul H. Ratz
Keyword(s):  
Strain Softening ◽  
Muscle Length ◽  
Free Solution ◽  
Passive Stiffness ◽  
Stress Softening ◽  
Induced Stress ◽  
Rhoa Kinase ◽  
Cross Links ◽  
Link Formation ◽  
Passive Muscle

Passive mechanical properties of strips of rabbit detrusor smooth muscle were examined and found by cyclic loading in a calcium-free solution to display viscoelastic softening and strain-induced stress softening (strain softening). Strain softening, or the Mullins effect, is a loss of stiffness attributed to the breakage of cross-links, and appeared irreversible in detrusor even after the return of spontaneous rhythmic tone during 120 min of incubation in a calcium-containing solution. However, 3 min of KCl or carbachol (CCh)-induced contraction permitted rapid regeneration of the passive stiffness lost to strain softening, and 3 μM of the RhoA kinase (ROK) inhibitor Y-27632 prevented this regeneration. The degree of ROK-induced passive stiffness was inversely dependent on muscle length over a length range where peak CCh-induced force was length independent. Thus rabbit detrusor displayed variable passive stiffness both strain- and activation-history dependent. In conclusion, activation of ROK by KCl or CCh increased passive stiffness softened by muscle strain and thereby attributed to cross-links that remained stable during tissue incubation in a calcium-free solution. Degradation of this signaling system could potentially contribute to urinary incontinence.

Relaxation of activated airway smooth muscle: relative potency of isoproterenol vs. tidal stretch

2001 ◽  
Vol 90 (6) ◽  
pp. 2306-2310 ◽  
Author(s):  
Alison Gump ◽  
Laura Haughney ◽  
Jeffrey Fredberg
Keyword(s):  
Smooth Muscle ◽  
Airway Smooth Muscle ◽  
Signal Transduction Pathway ◽  
Muscle Length ◽  
Active Force ◽  
Tidal Breathing ◽  
First Line ◽  
Relaxation Effects ◽  
High Concentrations ◽  
Multiplicative Effects

Both isoproterenol and tidal fluctuations of muscle length inhibit active force development in activated airway smooth muscle. In this study, we show that length fluctuations in the range of amplitudes expected during quiet tidal breathing produce force inhibition that is equipotent with high concentrations of isoproterenol. Active force fell to 50% of its isometric value when the amplitude of the tidal stretch was 4% of muscle length. The relaxing effects of length fluctuations were insensitive to the specific contractile agonist, suggesting that the mechanism of action is largely independent of the particular signal transduction pathway and lies instead at the level of bridge dynamics. This idea is reinforced by the results of combining the relaxation effects of tidal fluctuations with those produced by isoproterenol at all but the highest concentrations studied (10−5 M). Such a combination produces multiplicative effects, indicating largely separate modes of action. These observations suggest that the tidal muscle stretches that are attendant to spontaneous breathing comprise the first line of defense against bronchospasm and that tidal muscle stretches may be the most important of all known bronchodilating agencies.

Functional properties and connective tissue content of pediatric human detrusor muscle

2014 ◽  
Vol 307 (9) ◽  
pp. F1072-F1079 ◽  
Author(s):  
Navroop Johal ◽  
Dan N. Wood ◽  
Adrian S. Wagg ◽  
Peter Cuckow ◽  
Christopher H. Fry
Keyword(s):  
Smooth Muscle ◽  
Connective Tissue ◽  
Functional Properties ◽  
Biomechanical Properties ◽  
Detrusor Muscle ◽  
Detrusor Smooth Muscle ◽  
Passive Stiffness ◽  
Adult Tissue ◽  
Management Options ◽  
Intracellular Ca

The functional properties of human pediatric detrusor smooth muscle are poorly described, in contrast to those of adult tissue. Characterization is necessary for more informed management options of bladder dysfunction in children. We therefore compared the histological, contractile, intracellular Ca2+ concentration responses and biomechanical properties of detrusor biopsy samples from pediatric (3–48 mo) and adults (40–60 yr) patients who had functionally normal bladders and were undergoing open surgery. The smooth muscle fraction of biopsies was isolated to measure proportions of smooth muscle and connective tissue (van Gieson stain); in muscle strips, isometric tension to contractile agonists or electrical field stimulation and their passive biomechanical properties; in isolated myocytes, intracellular Ca2+ concentration responses to agonists. Pediatric detrusor tissue compared with adult tissue showed several differences: a smaller smooth muscle-to-connective tissue ratio, similar contractures to carbachol or α,β-methylene ATP when corrected for smooth muscle content, and similar intracellular Ca2+ transients to carbachol, α,β-methylene ATP, raised K+ concentration or caffeine, but smaller nerve-mediated contractions and greater passive stiffness with slower stress relaxation. In particular, there were significant atropine-resistant nerve-mediated contractions in pediatric samples. Detrusor smooth muscle from functionally normal pediatric human bladders is less contractile than that from adult bladders and exhibits greater passive stiffness. Reduced bladder contractile function is not due to reduced smooth muscle contractility but to greater connective tissue deposition and to functional denervation. Significant atropine resistance in pediatric detrusor, unlike in adult tissue, demonstrates a different profile of functional neurotransmitter activation. These data have implications for the management of pediatric bladder function by therapeutic approaches.

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