Tension changes during and after stretch in frog muscle fibres

1. Small fibre bundles from the semitendinosus muscles of the frog were stretched during tetanic stimulation, and the resulting tension changes were studied over a wide range of stretch velocities from 0.1 to 150 cm/sec (0.1-100 length/sec). The experiments were performed within the range of fibre lengths where the resting tension was negligible.2. With stretch velocities of more than 30 cm/sec (20 length/sec), the tension rose abruptly at first, and then started to fall while the stretch still continued, indicating the ;slip' of the contractile component. When the fibres were stretched at 80-150 cm/sec (70-100 length/sec), the tension fell quickly below the initial isometric level at the end of the stretch, and then began to rise again to the initial isometric value.3. Following stretches of 30-60 cm/sec (20-50 length/sec), the tension showed a delayed transient rise. The delayed rise of tension became more marked as the amount of stretch was increased.4. In some preparations, oscillatory tension changes were observed following stretches of 50-100 cm/sec (40-70 length/sec).5. The tension developed above the isometric level during moderate-velocity stretches of less than 15 cm/sec (10 length/sec) increased by lowering temperature, and showed a tendency to decay when the stretch velocity was suddenly reduced during a stretch.6. These results are discussed in relation to the sliding filament hypothesis, which provides an explanation for the findings of the present work.     

Effect of initial length on relations between oxygen uptake and load in dog muscle.

Oxygen uptake for brief tetanic contractions was calculated from measurements of blood flow and blood arteriovenous oxygen content differences. Each muscle preparation was pretested under isometric conditions to establish optimal length, Lo. After this one group of preparations performed afterload isotonic contractions at several loads with initial length, Li, less than Lo. The other groups of preparations performed similar contractions with Li greater than Lo. When Li was less than Lo, oxygen uptake for the highest load was always greater than oxygen uptake at the lowest load whereas intermediate loads were usually higher than both extremes. However, when Li was greater than Lo, oxygen uptake at the highest load was always less than oxygen uptake at the lowest load; again the intermediate loads were usually higher than both extremes. The data confirm and extend similar effects of initial length on heat production for contractions by amphibian muscles (7). It seems likely that the differences in initial lengths may account for the fact that the Fenn effect has not previously been observed in studies of mammalian skeletal muscle energetics.     

Dependence of energy output on force generation during muscle contraction.

It has been proposed that the energy (heat + work) output of an isometric twitch is determined by the force that is generated under conditions of invariant activation, irrespective of muscle length. To test the effect of length and force on total energy output, muscles were stretched by increments beyond the muscle length at which twitch force is maximum (LO) and then stimulated; energy output and force then were measured. These data were compared with isovelocity twitches in which stimulated muscles, initially at different lengths, shortened (near maximum velocity) a constant distance and then redeveloped tension at lengths less than LO. If energy liberation was determined by force generation, plots of energy output versus force produced would be parallel with isovelocity twitches liberating extra energy as shortening heat. As predicted, the ratio of the slopes (n = 13) of these relations, 0.98 +/- 0.02, was not different from 1 and the shortening heat coefficient (alphaF/Pot, measured from the difference in intercepts), 0.15 +/- 0.01, was near to the expected value. Therefore, energy liberation in twitches appears to be uniquely determined by force generation and not by muscle length.     

Mechanics of canine iliac artery smooth muscle in vitro.

Transmural pressure and external diameter were continuously recorded from intact segments of canine iliac artery and used to determine wall responses to maximal smooth muscle (SM) activation by norepinephrine (NE). Three different approaches were used:a) step inflations from low pressure following NE, B) slow, continuous inflation from low pressure following NE, and c) direct isometric and isobaric responses to NE. Passive pressure-diameter data were determined. The results show that active wall stress and diameter responses to NE determined using direct isometric and isobaric responses and from slow inflation responses (less than 1 mmHg/s) were not significantly different. Pressure-diameter and stress-strain curves determined using continuous (0.2 mmHg/s) and step pressure inflations after NE were not signficantly different. Pressure-diameter curves obtained at different inflation rates were not those expected from a simple viscoelastic material. The results suggest that slow inflation of iliac arteries with activated SM is a reasonable method for assessing contractile properties of SM. Furthermore, they also suggest that activation of iliac artery SM at high contractile element length (L greater than Lo) does not produce attenuated constriction responses.     

The mechanical response of active human muscle during and after stretch

Summary Five subjects contracted forearm supinator muscles which were stretched after development of maximal isometric torque. The ratio of torque at the end of stretch over isometric torque at that position was calculated as excess torque. Excess torque increased with stretch velocity and decreased with stretch amplitude, and it was not dependent upon final muscle length. The rate of decay of torque following stretch could not be shown to depend upon stretch variables.The absence of significant changes in myoelectric activity suggested that with high initial forces, reflex activity did not account for the observed changes. Time-constants of decay (0.15 s to 1.8 s) were much greater than time-constants of rise (approx. 0.07 s) of isometric torque at the same muscle length. This indicates that interaction of series elastic and contractile elements is not the sole cause of prolonged torque following stretch. It is concluded that stretch temporarily enhances the intrinsic contractile properties of a group of human muscles in a manner similar to, but quantitatively different from that seen in isolated muscle preparations.     

Force enhancement following muscle stretch of electrically stimulated and voluntarily activated human adductor pollicis

For electrically stimulated muscles, it has been observed that maximal muscle force during and after stretch is substantially greater than the corresponding isometric force. However, this observation has not been made for human voluntary contractions. We investigated the effects of active muscle stretch on muscle force production for in vivo human adductor pollicis ( n = 12) during maximal voluntary contractions and electrically induced contractions. Peak forces during stretch, steady-state isometric forces following stretch, and passive forces following muscle deactivation were compared to the corresponding isometric forces obtained at optimal muscle length. Contractions with different stretch magnitudes (10, 20, and 30 deg at a constant speed of 10 deg s⁻¹) and different speeds (10, 20, and 60 deg s⁻¹ over a range of 30 deg) were performed in triplicate in a random order, balanced design. We found three novel results: (i) there was steady-state force enhancement following stretch in voluntarily contracted muscles; (ii) some force enhancement persisted following relaxation of the muscle and (iii) force enhancement, for some stretch conditions, exceeded the maximum isometric force at optimal muscle length. We conclude from these results that voluntary muscle contraction produces similar force enhancement to that observed in the past with electrically stimulated preparations. Therefore, steady-state force enhancement may play a role in everyday movements. Furthermore, these results suggest that non-uniformities in sarcomere length do not, at least not exclusively, account for the force enhancement following active muscle stretch, and that the stretch magnitude-dependent passive force enhancement observed here may be responsible for the enhancement of force above the isometric reference force at optimal muscle length.     

The series elastic component of frog gastrocnemius

1. The force-extension curve of the series elastic elements of the frog gastrocnemius has been determined up to the force attained during stretching by means of the isotonic quick-release method, modified in order to allow the release of the muscle immediately after stretching.2. The series compliance decreases progressively up to a stress value of about 2 kg/cm(2) and then it remains constant up to the maximal values of stress attained (about 10 kg/cm(2)).3. The lengthening of the series elastic elements when the stress rises to its full isometric value (P(0)l(0)/M = 5.2 kg/cm(2)) is about 3% of the muscle resting length, l(0). The Young's modulus in the linear part of the diagram is 294 kg/cm(2).4. The elastic energy stored up to P(0) is on average 55 g cm/g; an additional amount of 63 g cm/g is stored during stretching the contracted muscle.     

Regional distribution of blood flow in calf muscles of rat during passive stretch and sustained contraction.

The regional distribution and number of microspheres in the calf muscles of rat has been studied during isometric sustained contraction and in stretched uncontracted muscles in situ. Carbonized microspheres, 15 +/- 5 mum, were injected into the aortic arch and muscle blood flow arrested 6 sec later. The calf muscles were freeze sectioned (12 slices of 40 mum) and the microspheres counted microscopically. The microsphere concentration in the gastrocnemius and plantaris muscles during rest was 4.6 +/- 1.6 spheres/mm3 (mean +/- S.E.). One min after a standardized exercise programme the sphere concentration was increased to 20.5 +/- 3.9 spheres/mm3. At increasing force of contraction following the standard exercise programme, the microsphere concentration fell from 11.6 +/- 2.5 at 25% of maximal force of contraction (MFC) to 2.2 +/- 0.6 spheres/mm3 at 100% MFC (5.6 kg/cm2). Corresponding measurements in stretched, uncontracted muscles showed a similar fall in microsphere concentration in the central inner zone and in the peripheral outer zone was slightly higher than unity (1.08-1.16) in muscles at rest and at light postexercise hyperemia. At 75 and 100% MFC the ratio was 0.76 +/- 0.07 and 0.57 +/- 0.13, significantly lower than unity. Stretching of the uncontracted muscle group to 175% MFC reduced the ratio towards zero. The greater reduction in blood flow to the inner central zone of contracted calf muscles shown by microsphere distribution was confirmed by measurement of 125 I-antipyrine distribution. These results show an increased resistance against blood flow during active contraction or stretching of the calf muscles, most pronounced in the central inner zone at high tensions.     

Dynamic stiffness of rabbit mesotubarium smooth muscle: effect of isometric length

The dynamic stiffness of mesotubarium smooth muscle from nonpregnant adult rabbits was measured continuously during isometric contraction by applying small (0.5 percent of the muscle length) sinusoidal length perturbations and measuring the amplitude and phase of the resulting tension perturbations. Stiffness during contraction was directly proportional to muscle tension; during relaxation stiffness at all tensions was significantly increased as compared to the values encountered during the rise of tension. Peak isometric tension and dynamic stiffness (determined at a common tension level) both decreased at shorter muscle lengths; the relative falloff in stiffness was significantly less than the tension decrease. Varying levels of muscle activation (obtained by changing stimulus strength and by applying quick releases to active muscle) had little effect on the measured elastic modulus. Comparisons of these results with published data on single-cell contractile properties imply a cellular locus for a portion of the measured stiffness.     

An analysis of the role of calcium in facilitation at the frog neuromuscular junction

1. The force-velocity relationship and the stress-strain curve of the so-called series elastic component (s.e.c.) of frog sartorius, semitendinosus and gastrocnemius have been determined during shortening against a given force (isotonic quick-release) and at high speed (controlled release): (a) from a state of isometric contraction and (b) after stretching of the contracted muscle. In both cases the muscle was released from the same length: this was usually slightly greater than the muscle's resting length.2. The muscle released immediately after being stretched is able to shorten against a constant force, P, equal to or even greater than the isometric force, P(0), at the same length. When the force P applied to the muscle is reduced below P(0) the velocity of shortening is greater after stretching, and the force-velocity curve is therefore shifted along the velocity axis: the shift is maximal when P is near to P(0) and it decreases rapidly with decreasing P.3. The extent of shortening of the s.e.c. required to make the force fall from P(0) to zero is 50-100% greater when the muscle is released immediately after stretching than when it is released from a state of isometric contraction. This difference is found by using either the controlled release method or the isotonic quick-release method.4. If a time interval is left between the end of stretching and the onset of shortening of the contracted muscle (controlled release method), the length change of the s.e.c., for a given fall of the force, is reduced and approaches that taking place when the muscle is released from a state of isometric contraction.5. Curare does not affect the results described above, indicating that these do not depend on modification of the neuromuscular transmission.6. It is concluded that stretching a contracted muscle modifies temporarily: (a) its elastic characteristics, as shown by the greater amount of mechanical energy released for a given fall of the force at the muscle's extremities, and (b) its contractile machinery, as it is suggested by the change of the force-velocity relationship.     

The effect of long-term stimulation of fast muscles on their blood flow,metabolism and ability to withstand fatigue

Chronic stimulation of fast rabbit muscles (tibialis anterior, extensor digitorum longus and the peroneal muscle group) at a frequency naturally occurring in nerves to slow muscles increased their ability to withstand fatigue. Isometric tension decreased during a 10-min period of contractions at 4 Hz by 75% in control muscles, but only 55% in muscles chronically stimulated for 4 days, and 23% in muscles stimulated for 28 days. Chronic stimulation had little effect on resting blood flow, oxygen or glucose consumption. The output or consumption of lactate and free fatty acids (FFA) at rest were also unaffected. The glycogen content was regularly increased, and was apparent after only 2 days of stimulation. The activity of fatty acid activating enzyme was increased after 28 days. During a 10-min period of isometric contractions at 4 Hz, there was a markedly greater increase in blood flow and oxygen consumption in muscles stimulated for 14-28 days than in control muscles; lactic acid output was lower in muscles stimulated for 28 days, and the uptake of FFA was significantly higher. It is therefore suggested that muscles chronically stimulated for 14-28 days use fats as the main source of energy during isometric contractions. The predominantly oxidative metabolism is probably facilitated by the higher density of capillaries. The latter also enables more efficient delivery of oxygen, and therefore smaller fatiguability, already after 4 days of chronic stimulation.     

A-band length, striation spacing and tension change on stretch of active muscle.

1. Single muscle fibres of the frog were stretched during tetanus and filmed down the interference microscope. 2. Sarcomere lengths and A- and I-band widths were measured from cine films taken of the experimental sequences. 3. When a fibre was stretched during a tetanus, its A-band widths remained constant while its I-band widths changed according to the extent of the stretch. This behaviour is identical with that of a fibre stretched at rest. 4. Sarcomere lengths remained uniform along the fibre during a tetanus plus stretch, increasing as the I-band widths increased when the fibre was stretched. 5. At sarcomere lengths longer than LPmax (the length corresponding to greatest isometric tetanus tension) where the isometric tension diminishes as the fibre is lengthened, if the stretch was imposed during a tetanus the tension was higher after the stretch than before, showing a plateau which lasted for the duration of the tetanus. 6. This effect increased with longer sarcomere lengths and was not due to increased resting tension.     

Length-dependent sensitivity at lengths greater than Lmax in vascular smooth muscle

Previous work has shown that vascular smooth muscle sensitivity depends on muscle length (arterial circumference) at lengths equal to and less than that for maximum active force (Lmax). In the present study dose-response curves were obtained from dog anterior tibial artery rings at lengths equal to or longer than Lmax. The curves were compared with dose-response curves obtained at lengths less than Lmax. The agonist concentration for half maximal response (ED50) was determined by graphical estimation and by calculation from a best-fit curve. The results show that with norepinephrine (NE) stimulation 1) ED50 decreased significantly at each step when the rings were stretched from Lmax to 1.15 Lmax and then to 1.30 Lmax; 2) ED50 increased significantly when length was decreased from 1.15 to 1.00 Lmax; 3) ED50 decreased significantly at each step when the rings were stretched from 0.70 Lmax to Lmax and then to 1.30 Lmax; and 4) for NE concentration greater than the ED50 at Lmax, active stress was significantly higher at Lmax than at 0.70 Lmax or 1.30 Lmax. For an NE concentration less than the ED50 at Lmax, the active stress at 1.30 Lmax was higher than the active stress at Lmax and at 0.70 Lmax. The results show that sensitivity of vascular smooth muscle continually increases with stretch and does not have a maximum at the length for maximum active force.     

Oxygenation and perfusion of rabbit tibialis anterior muscle subjected to different patterns of electrical stimulation

Dual amperometric microelectrodes were used to measure local pO₂ and perfusion at multiple sites in the fast-twitch tibialis anterior muscles of anaesthetized rabbits. Six muscles were stimulated continuously at 10, 5, or 2.5 Hz. For all three frequencies, perfusion declined to about 50% of resting levels and recovered after stimulation. These changes corresponded to a rise followed by a fall in extracellular pO₂. The highest levels of pO₂ were reached during stimulation at 10 Hz. Eight muscles were stimulated tetanically at 100 Hz for 200 ms with duty cycles that were varied between 1.3 and 20.0%. Perfusion rose to 8.7 ± 2.0 ml s^–1 100 g^–1 at a duty cycle of 5% and declined with further increases in duty cycle. pO₂ was depressed for duty cycles less than 10% but rose above resting levels at higher duty cycles. It is suggested that the paradoxical combination of elevated pO₂ and depressed perfusion is attributable to stimulation conditions that exceed the oxygen transport capacity of a fast muscle.     

Activation heat, activation metabolism and tension-related heat in frog semitendinosus muscles

1. Frog semitendinosus muscles were stretched to various lengths beyond the rest length (l(0)) and their initial heat and isometric tension production were measured.2. As the overlap between the thick and thin filaments is reduced, the initial twitch heat and tension decline in a linear manner. At a point at which the twitch tension approaches zero, the initial heat is 30% of that seen at l(0). It is concluded that this heat is the activation heat and reflects the energetics of calcium release and reaccumulation. The initial heat at shorter sarcomere lengths appears to be the sum of the activation heat plus a heat production associated with the interaction of the thick and thin filaments.3. A similar relationship between heat and tension production is seen in tetanic contractions.4. The time course of activation heat production in a twitch can be resolved into two phases: a temperature insensitive (Q(10) < 1.3) ;fast' phase (with a time constant of 45 msec) and a temperature sensitive (Q(10) = 2.8) ;slow' phase (with a time constant of 330 msec at 0 degrees C).5. Measurements of the creatine phosphate (PC) hydrolysis by muscles contracting isometrically at various muscle lengths at and beyond l(0), indicate an enthalpy change of -11.2 kcal/mole PC hydrolysed. The enthalpy change for the ATP hydrolysis by muscles stretched so that little or no tension was produced with stimulation was -9.9 kcal/mole ATP hydrolysed. It is concluded that the net activation heat is produced by the hydrolysis of PC or ATP.     

Regional Distribution of Blood Flow in Calf Muscles of Rat during Passive Stretch and Sustained Contraction

The regional distribution and number of microspheres in the calf muscles of rat has been studied during isometric sustained contraction and in stretched uncontracted muscles in situ. Carbonized microspheres, 15 ± 5 μm, were injected into the aortic arch and muscle blood flow arrested 6 sec later. The calf muscles were freeze sectioned (12 slices of 40μm) and the microspheres counted microscopically. The microsphere concentration in the gastrocnemius and plantaris muscles during rest was 4.6 ± 1.6 spheres/mm³ (mean ± S.E.). One min after a standardized exercise programme the sphere concentration was increased to 20.5 ± 3.9 spheres/mm³. At increasing force of contraction following the standard exercise programme, the microsphere concentration fell from 11.6 ± 2.5 at 25% of maximal force of contraction (MFC) to 2.2 ± 0.6 spheres/mm³ at 100% MFC (5.6 kg/cm²). Corresponding measurements in stretched, uncontracted muscles showed a similar fall in microsphere concentration when stretch was increased from 50 to 175% MFC. The ratio between microsphere concentration in the central inner zone and in the peripheral outer zone was slightly higher than unity (1.08-1.16) in muscles at rest and at light postexercise hyperemia. At 75 and 100% MFC the ratio was 0.76 ± 0.07 and 0.57 ± 0.13, significantly lower than unity. Stretching of the uncontracted muscle group to 175% MFC reduced the ratio towards zero. The greater reduction in blood flow to the inner central zone of contracted calf muscles shown by microsphere distribution was confirmed by measurement of ¹²⁵I-antipyrine distribution. These results show an increased resistance against blood flow during active contraction or stretching of the calf muscles, most pronounced in the central inner zone at high tensions.     

The resistance to blood flow in the gastrocnemius of the dog during sustained and rhythmical isometric and isotonic contractions

Summary The effect of sustained isometric and isotonic contractions on the resistance to blood flow was studied in isolated autoperfused electrically stimulated gastrocnemius muscles of anesthetized dogs. To prevent autoregulation caused by the contraction from interferring with the mechanical effects of contraction on the resistance to flow, local vasomotor tone was eliminated by dilating the vessels maximally with vasodilator drugs.Passive stretching of the muscles increased the resistance to flow in proportion to the increase of muscle length.Sustained isometric contractions increased the resistance to flow markedly in proportion to the developed tension. In some experiments powerful isometric contractions nearly completely stopped the flow through the muscle. It could be calculated that working capacity of the muscle was limited by this mechanical inhibition of flow even during weak isometric contractions.Sustained isotonic contractions increased resistance to flow not at all or insignificantly when the contraction was less than 60% of the maximum of the isotonic shortening. Isotonic contractions of more than 60% of maximal shortening increased resistance to flow markedly, but vessels were never completely occluded. That means that isometric contractions impeded flow much more than isotonic contractions.Increasing the arterial blood pressure significantly reduced the increase of resistance to flow caused by isometric or isotonic contractions. Maximum of force as well as maximum of shortening of the muscle was uninfluenced by the raised perfusion pressure, but endurance was improved by an increased blood supply to the gastrocnemius.Rhythmical isotonic and isometric tetanic contractions did not increase mean resistance to blood flow significantly. That means that the inhibition of inflow into the muscle during the contractions was compensated by a massage effect on the vessels. The net effect of rhythmical contraction on extravascular support, therefore, was zero.Supported by the Deutsche Forschungsgemeinschaft     

Influence of muscle length on the force-velocity relation of K+-contractures in smooth muscle from rabbit urinary bladder

Force-velocity relations of K+-contractures of longitudinal smooth muscle from rabbit urinary bladder were studied by isotonic quick release at 37 degrees C. In order to minimize the influence of parallel elasticity the study was limited to the rising part of the length-tension curve. The force-velocity data fitted well with Hill's equation. The in situ length of the strip at a bladder volume of 10 ml is called L10. This length is 50% of that at which maximum active tension is developed. At L10 Vmax was 0.29 muscle lengths per second and it was estimated to be 0.36 lengths/s at optimum length. Constant b in Hill's equation had a value of 0.052 L10/s and it was unaffected by length changes over the interval 0.69 L10-1.44L10. At L10 a/Po was 0.17. In the interval given above, a/Po decreased with increasing length in proportion to the increase in Po, indicating that a was also length independent. According to Hill's equation [V = b(Po - P)/(P + a)], V should increase in proportion to (Po - P) when the muscle length is increased if a and b are constants. Such a linear relation was found at shorter lengths but at lengths close to or at the length for maximum active tension, V increased more than (Po - P). Two possible explanations were considered; firstly that b/(P + a) increased, and secondly that the load on the contractile element could be less that P due to an influence of the considerable tension in the parallel elastic element at these lengths. The series elastic recoil of the active muscle amounted to 3-4% of the muscle length when released to zero tension.     

Muscular fatigue and rate of tension development

Summary The effects of long-term fatigue upon maximal force and peak rate of tension development (PRTD) (dF/dt max) are studied in man (elbow flexors), in the rat (pseudo-isolated gastrocnemius muscle) and in the frog (isolated sartorius muscle). The muscles are fatigued by voluntary anisometric anisotonic contractions against an elastic resistance in man, and by maximal tetanic contractions in the frog and the rat. In man, the excitation level of the muscle is controlled by the integrated surface EMG of the biceps brachii. In the animals, the muscles are stimulated by a neurostimulator. The PRTD and the maximal isometric force are measured during fatigue tests.In man, frog and rat, the maximal voluntary isometric torque or the maximal force and the PRTD decrease initially more or less rapidly according to the power developed during the fatigue process, and then less rapidly. The relationship between PRTD and maximal force is linear in the animals and curvilinear in man.The variations of maximal force and PRTD are discussed in relation to the level of excitation of the muscles and of the composition in different motor units types and their spatio-temporal recruitment. From a biomechanical point of view, it seems necessary to study the behavior of the series elastic component during the evolution of long term fatigue.     

Muscle economy of isometric contractions as a function of stimulation time and relative muscle length

For rat medial gastrocnemius muscle economy (i.e. the ratio of time integral of force and total energy-rich phosphate consumption) was calculated. Muscles in situ at 35°C were stimulated to perform either one continuous or several repetitive isometric contractions at one muscle length in the range from 70% to 130% of optimum muscle length for force generation. Whereas during one continuous contraction economy increased, no differences in economy were found between 6, 12 or 18 successive contractions. Economy during intermittent exercise was always lower than during continuous exercise. The difference in economy is a result of different rates of metabolism, whereas no difference was found for force generation. Economy was highest at optimum muscle length for force generation and decreased at muscle lengths smaller as well as greather than optimum muscle length. Force-dependent energy consumption was calculated by substracting the force-independent part (obtained by extrapolation) from total energy consumption. The calculated force produced per mol force-dependent energy-rich phosphate consumption was similar in muscles stretched beyond optimum length. In contrast, a decreasing amount of force per mol force-dependent energy-rich phosphate consumption was observed at lengths smaller than optimum length.