Dynamics of efferent control of muscular contraction. Determination of transition processes: External load — Muscle length

Transition processes of the change in length of the soleus, gastrocnemius, and plantaris muscles during stepwise transition from isometric to isotonic contraction were investigated in acute experiments on anesthetized cats using a constant frequency of efferent stimulation. Stimulation was distributed over three to six distal filaments of the divided ventral roots L7-S1. Using two-component approximation of transition processes by reactions of inertia-free and aperiodic first-order components, connected in parallel, the dynamic characteristics of the effect of an external load on length of an active muscle were determined. Nonlinear properties of muscular contraction were manifested as a complex relationship between the time constant and weight of the aperiodic component and the amplitude of the input signals. Time constants and weight of the aperiodic component during muscle shortening were significantly less than during lengthening. Average limiting values of the time constant with a reduction in change of the external load, based on the results of many experiments, were 1.38 sec for the soleus muscle during shortening and 0.39 sec during lengthening, and for the fast muscles the times were 0.55 and 0.25 sec, respectively. The functional significance of nonlinear dynamic properties of muscles is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 17, No. 3, pp. 334–343, May–June, 1985.     

Three-Dimensional Muscle Architecture and Comprehensive Dynamic Properties of Rabbit Gastrocnemius,Plantaris and Soleus: Input for Simulation Studies

The vastly increasing number of neuro-muscular simulation studies (with increasing numbers of muscles used per simulation) is in sharp contrast to a narrow database of necessary muscle parameters. Simulation results depend heavily on rough parameter estimates often obtained by scaling of one muscle parameter set. However, in vivo muscles differ in their individual properties and architecture. Here we provide a comprehensive dataset of dynamic (n = 6 per muscle) and geometric (three-dimensional architecture, n = 3 per muscle) muscle properties of the rabbit calf muscles gastrocnemius, plantaris, and soleus. For completeness we provide the dynamic muscle properties for further important shank muscles (flexor digitorum longus, extensor digitorum longus, and tibialis anterior; n = 1 per muscle). Maximum shortening velocity (normalized to optimal fiber length) of the gastrocnemius is about twice that of soleus, while plantaris showed an intermediate value. The force-velocity relation is similar for gastrocnemius and plantaris but is much more bent for the soleus. Although the muscles vary greatly in their three-dimensional architecture their mean pennation angle and normalized force-length relationships are almost similar. Forces of the muscles were enhanced in the isometric phase following stretching and were depressed following shortening compared to the corresponding isometric forces. While the enhancement was independent of the ramp velocity, the depression was inversely related to the ramp velocity. The lowest effect strength for soleus supports the idea that these effects adapt to muscle function. The careful acquisition of typical dynamical parameters (e.g. force-length and force-velocity relations, force elongation relations of passive components), enhancement and depression effects, and 3D muscle architecture of calf muscles provides valuable comprehensive datasets for e.g. simulations with neuro-muscular models, development of more realistic muscle models, or simulation of muscle packages.     

Mechanical deficit persists during long-term muscle hypertrophy

Hypotheses were tested that the deficit in maximum isometric force normalized to muscle cross-sectional area (i.e., specific Po, N/cm2) of hypertrophied muscle would return to control value with time and that the rate and magnitude of adaptation of specific force would not differ between soleus and plantaris muscles. Ablation operations of the gastrocnemius and plantaris muscles or the gastrocnemius and soleus muscles were done to induce hypertrophy of synergistic muscle left intact in female Wistar rats (n = 47) at 5 wk of age. The hypertrophied soleus and plantaris muscles and control muscles from other age-matched rats (n = 22) were studied from days 30 to 240 thereafter. Po was measured in vitro at 25 degrees C in oxygenated Krebs-Ringer bicarbonate. Compared with control values, soleus muscle cross-sectional area increased 41-15% from days 30 to 240 after ablation, whereas Po increased 11 and 15% only at days 60 and 90. Compared with control values, plantaris muscle cross-sectional area increased 52% at day 30, 40% from days 60 through 120, and 15% at day 240. Plantaris muscle Po increased 25% from days 30 to 120 but at day 240 was not different from control value. Changes in muscle architecture were negligible after ablation in both muscles. Specific Po was depressed from 11 to 28% for both muscles at all times. At no time after the ablation of synergistic muscle did the increased muscle cross-sectional area contribute fully to isometric force production.     

Analysis of muscle movement during frequency-modulated activation of efferents

The basic principles governing trajectories of change in muscle length (henceforth referred to as "movement") were analyzed at varying rates of distributed afferent stimulation during experiments on the soleus and plantaris muscles in unanesthetized cats. The theoretical possibility of describing evoked movements within the context of a model having nonlinear hysteresis properties and dependence of dynamic parameters on direction of movement were demonstrated. A difference in static transitions between muscle contraction and lengthening was found and vice versa and retardation of movement at the start of lengthening reaction (induced by a reduced efferent stimulation rate) was more pronounced. Interaction was discovered between two disruptive influences: changes in the rate of efferent stimulation and external load, mainly due to hysteresis effects of muscle contraction. The trajectory of movement produced by alteration in one of the inputs at work (external load or afferent stimulation) is associated with the lead-up to the muscle motion, irrespective of the reason inducing the foregoing movement. Functional implications of the nonlinear dynamics of muscular contraction are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 21, No. 4, pp. 443–450, July–August, 1989.     

Adaptation in synergistic muscles to soleus and plantaris muscle removal in the rat hindlimb.

Although the soleus muscle comprises only 6% of the ankle plantar flexor mass in the rat, a major role in stance and walking has been ascribed to it. The purpose of this study was to determine if removal of the soleus muscle would result in adaptations in the remaining gastrocnemius and plantaris muscles due to the new demands for force production imposed on them during stance or walking. A second purpose was to determine whether the mass or the fiber type of the muscle(s) removed was a more important determinant of compensatory adaptations. Male Sprague-Dawley rats underwent bilateral removal of soleus muscle, plantaris muscle, or both muscles. For comparison, compensatory hypertrophy was induced in soleus and plantaris muscles by gastrocnemius muscle ablation. After forty days, synergist muscles remaining intact were removed. Mass, and oxidative, glycolytic, and contractile enzyme activities were determined. Despite its role in stance and slow walking, removal of the soleus muscle did not elicit a measurable alteration in muscle mass, or in citrate synthase, lactate dehydrogenase, or myofibrillar ATPase activity in gastrocnemius or plantaris muscles. Similarly, removal of the plantaris muscle, or soleus and plantaris muscles, had no effect on the gastrocnemius muscle, suggesting that this muscle was able to easily meet the new demands placed on it. These results suggest that amount of muscle mass removed, rather than fiber type, is the most important stimulus for compensatory hypertrophy. They also suggest that slow-twitch motor units in the gastrocnemius muscle play an important role during stance and locomotion in the intact animal.     

Changes in lipid levels of three skeletal muscles following denervation

Nonpolar and polar lipids extracted from denervated rat gastrocnemius, plantaris, and soleus muscles were measured 7–9 days after unilateral sciatic nerve transection. The contralateral muscle (CCON) was used to obtain control lipid levels. After denervation changes in lipid concentrations were found in all three muscles. These alterations in lipid levels were generally in the same direction but not to the same extent. The change in total nonpolar lipids (NL) was an increase in soleus > gastrocnemius > plantaris concentration. This change in lipid concentration was more apparent than real since the wet weight of muscle was decreased after denervation. Since polar lipid (PL) concentrations were not increased under these conditions of muscle weight loss, an actual decrease of polar lipids after denervation may be inferred.In contrast to the other two muscles, a marked difference was noted for polar lipids of denervated gastrocnemius muscle. An unidentified spot near the origin was detected. This area is the location of a nerve sprouting factor(s). The compound(s) was not detectable for the other two muscles. When the gastrocnemius from an unoperated animal rather than a CCON muscle was used as a benchmark, slight increases were found for total nonpolar, polar, and plasmalogen fractions following denervation. The changes for individual lipid fractions were less definable, except for the significant increase for the unknown polar compound near the origin. This spot was noted in extracts from CCON and DEN muscles but not in untouched control muscle. The CCON gastrocnemius muscle is therefore a poor control for determining effects of denervation on lipid levels and perhaps other biochemical parameters as well.     

Hindlimb unloading-induced muscle atrophy and loss of function: protective effect of isometric exercise.

The primary objective of this study was to determine the effectiveness of isometric exercise (IE) as a countermeasure to hindlimb unloading (HU)-induced atrophy of the slow (soleus) and fast (plantaris and gastrocnemius) muscles. Rats were assigned to either weight-bearing control, 7-day HU (H7), H7 plus IE (I7), 14-day HU (H14), or H14 plus IE (I14) groups. IE consisted of ten 5-s maximal isometric contractions separated by 90 s, administered three times daily. Contractile properties of the soleus and plantaris muscles were measured in situ. The IE attenuated the HU-induced decline in the mass and fiber diameter of the slow-twitch soleus muscle, whereas the gastrocnemius and plantaris mass were not protected. These results are consistent with the mean electromyograph recordings during IE that indicated preferential recruitment of the soleus over the gastrocnemius and plantaris muscles. Functionally, the IE significantly protected the soleus from the HU-induced decline in peak isometric force (I14, 1.49 +/- 0.12 vs. H14, 1.15 +/- 0.07 N) and peak power (I14, 163 +/- 17 vs. H14, 75 +/- 11 mN.fiber length.s-1). The exercise protocol showed protection of the plantaris peak isometric force at H7 but not H14. The IE also prevented the HU-induced decline in the soleus isometric contraction time, which allowed the muscle to produce greater tension at physiological motoneuron firing frequencies. In summary, IE resulted in greater protection from HU-induced atrophy in the slow soleus than in the fast gastrocnemius or plantaris.     

Some hormonal factors (hypophysectomy, castration and testosterone administration) modifying the course of "compensatory" muscle hypertrophy in the rat.

1. Maximum compensatory hypertrophy of the soleus and plantaris muscle in male rats is attained seven days after tenotomy of the gastrocnemius muscle (39% and 9% respectively). When tenotomy of the gastrocnemius was performed seven days ater hypophysectomy, hypertrophy in these two muscles was aproximately half that found in control animals. 2. After 81-day castration of young male rats the weight of the saleus and plantaris was reduced and hypertrophy following tenotomy of the gastrocneumius muscle did not develop. 3. Chronically castrated rats received testosterone two weeks prior to tenotomy of the gastrocnemius and a week during the muscle hypertrophy phase. Hypertrophy of the soleus in castrated rats which had received testosterone seven days after tenotomy of the gastrocnemius was 25% as compared with muscles of castrated animals. The corresponding value in the plantaris muscle was 10%. 4. These results indicate that even calf muscles of the rat, namely the soleus and plantaris muscles, are significantly affected by testosterone under these conditions, although it is not, as yet, clear whether its action is direct or indirect.     

Technique for interpretation of electromyography for concentric and eccentric contractions in gait

We present a technique to combine muscle shortening and lengthening velocity information with electromyographic (EMG) profiles during gait. A biomechanical model was developed so that each muscle's length could be readily calculated over time as a function of angles of the joints it crossed. The velocity of shortening and lengthening of the muscle fiber was then calculated, and with computer graphics this information was overlaid on the EMG profiles. Thus, researchers and clinicians were not only able to interpret the processed EMG signal as level of activity (tension) but also to gain insight as to the muscles' role as generators (muscle shortening) or absorbers (muscle lengthening) of energy. Six common muscles are documented, using database profiles; soleus (SOL), medial gastrocnemius (MG), tibialis anterior (TA), vastus lateralis (VL), rectus femoris (RF), and semitendinosus (ST). The protocol thus demonstrates a relatively simple technique for calculating muscle fiber velocity and for combining that velocity information with EMG activity profiles.     

Nonlinear characteristics of changes in active muscle length

The principle nonlinear characteristics of changes in the length of active (soleus, gastrocnemius, and plantaris) muscle resulting from controlled changes in external load were examined during acute experiments on anesthetized cats. Summation of successive muscle responses to repetitive phased changes in load was shown to be absent due to hysteresis effects; this does not satisfy the principles of superposition and leads to an important functional result: the muscle exerts a stabilizing effect on overall motor system dynamics, limiting unwanted shifts in joint angles during variation in external load. A relationship between the trajectory profile of change in muscle length and the lead-up to the movement arises due to muscle contraction hysteresis. Velocity at the initial stage of movement was always higher when the latter was preceded by motion in the same direction. The functional significance of the nonlinear properties of active muscle movement accompanying changing external load is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 20, No. 6, pp. 736–743, November–December, 1988.     

Biochemical response to chronic shortening in unloaded soleus muscles

One leg of tail-casted suspended rats was immobilized in a plantar-flexed position to test whether chronic shortening of posterior leg muscles affected the metabolic response to unloading. The immobilized plantaris and gastrocnemius muscles of these animals showed approximately 20% loss of muscle mass in contrast to simply a slower growth rate with unloading. Loss of mass of the soleus muscle during suspension was not accentuated by chronic shortening. Although protein degradation in the isolated soleus muscle of the plantar-flexed limb was slightly faster than in the contralateral free limb, this difference was offset by faster synthesis of the myofibrillar protein fraction of the chronically shortened muscle. Total adenine nucleotides were 17% lower (P less than 0.005) in the chronically shortened soleus muscle following incubation. Glutamate, glutamine, and alanine metabolism showed little response to chronic shortening. These results suggest that, in the soleus muscle, chronic shortening did not alter significantly the metabolic responses to unloading and reduced activity.     

Changes in myosin heavy chain isoform expression of overloaded rat skeletal muscles

• 1.1. The effect of functional overload produced by tenotomy of synergistic gastrocnemius muscle on the expression of myosin heavy chain (MHC) isoforms in the plantaris and soleus muscles of the rat was studied using gradient sodium dodecyl sulfate-acrylamide gel electrophoresis.
• 2.2. Five weeks tenotomy, the plantaris and soleus muscle weights induced by tenotomy of the gastrocnemius muscle were 44.3% (P < 0.005) and 37.4% (P < 0.005), respectively, heavier than the contralateral control muscles.
• 3.3. Although four types of MHC isoforms were observed in both control and experimental plantaris, the percentage of MHC isoforms in the control and experimental muscles differed; the hypertrophied plantaris muscle contained more HCI (P < 0.05), HCIIa and HCIId (P < 0.05) and less HCIIb (P < 0.05) than the control muscle.
• 4.4. The control soleus muscle contained two MHC isofonns, HCI and HCIIa. However, there was only a single HCI isoform in the hypertrophied soleus muscle.
• 5.5. These results indicate that overloading a skeletal muscle by removing its synergists produces not only the muscle hypertrophy but also the changes in the expression of MHC isofonns.

     

Effects of elastic loads on the contractions of cat muscles

The nerves to plantaris and soleus muscles in the cat were stimulated with maximal single shocks and with random stimulus trains which produced partially fused contractions. In order to obtain information on the mechanism of muscular contraction, the effects of allowing the muscles to shorten against various elastic loads were studied in the time domain and in the frequency domain. When springs of increasing stiffness were placed in series with the muscle, the twitch tension increased greatly. The gain of the frequency response curve was also much greater with stiffer springs. The shape of the frequency response curve for plantaris muscle could usually be described by that expected for a second-order system with two real time constants or rate constants. The rate constants changed in qualitatively similar ways in response to increased stiffness of an elastic load, increased muscle length and increased mean rate of nerve stimulation. These results are in agreement with the hypothesis that the linear responses of muscles working against elastic loads are determined by the values of two rate constants. Thus, of the many processes associated with contraction, only two are rate-limiting: one associated with the viscoelastic properties of muscle and the second associated with the reuptake of Ca into the sarcoplasmic reticulum. Non-linear aspects of muscular contraction are also discussed. These are more prominent in soleus muscle than in plantaris muscle.Graduate student of the Medical Research Council of Canada.Formerly a Post-doctoral Fellow of the Muscular Dystrophy Association of Canada.     

Blood flow and glycogen use in hypertrophied rat muscles during exercise

Previous findings suggest that skeletal muscle that has enlarged as a result of removal of synergistic muscles has a similar metabolic capacity and improved resistance to fatigue compared with normal muscle. The purpose of the present study was to follow blood flow and glycogen loss patterns in hypertrophied rat plantaris plantaris and soleus muscles during treadmill exercise to provide information on the adequacy of perfusion of the muscles during in vivo exercise. Thirty days following surgical removal of gastrocnemius muscle, blood flows (determined with radiolabeled microspheres) and glycogen concentrations were determined in all of the ankle extensor muscles of experimental and sham-operated control rats during preexercise and after 5-6 min of treadmill exercise at 15 m/min. There were no differences (P greater than 0.05) in blood flows per unit mass or glycogen concentrations between control and hypertrophied plantaris or soleus muscles at either time, although both muscles were larger (P less than 0.05) in the experimental group (plantaris: 95%; soleus: 40%). None of the other secondary ankle extensor muscles (tibialis posterior, flexor digitorum longus or flexor hallicus longus) hypertrophied in response to removal of gastrocnemius. These results provide indirect evidence that O2 delivery in the enlarged muscles is not compromised during low-intensity treadmill exercise due to limited perfusion.     

Conversion of rat muscle fiber types. A time course study

Rats were used in this study to determine the time course of conversion of muscle fiber types. The right or left gastrocnemius muscle was removed thereby causing an overload on the ipsilateral soleus and plantaris muscles. The contralateral limb served as a control. The type II to type I fiber conversion was followed histochemically in the soleus and plantaris muscles for one to six weeks following surgery. Muscle sections were stained for myofibrillar actomyosin ATPase and NADH tetrazolium reductase. The type I population in the soleus muscle was 99.3% six weeks after synergist removal. The plantaris muscle underwent a two fold increase in the percentage of type I fibers after six weeks. Transitional fibers were prominent in the plantaris muscle and reached their peak at 4% (P less than 0.05) of the total population, four weeks after surgery.     

Force-length properties and functional demands of cat gastrocnemius, soleus and plantaris muscles.

The purpose of this study was to measure isometric force-length properties of cat soleus, gastrocnemius and plantaris muscle-tendon units, and to relate these properties to the functional demands of these muscles during everyday locomotor activities. Isometric force-length properties were determined using an in situ preparation, where forces were measured using buckle-type tendon transducers, and muscle-tendon unit lengths were quantified through ankle and knee joint configurations. Functional demands of the muscles were assessed using direct muscle force measurements in freely moving animals. Force-length properties and functional demands were determined for soleus, gastrocnemius and plantaris muscles simultaneously in each animal. The results suggest that isometric force-length properties of cat soleus, gastrocnemius and plantaris muscles, as well as the region of the force-length relation that is used during everyday locomotor tasks, match the functional demands.     

Conversion of rat muscle fiber types

Summary Rats were used in this study to determine the time course of conversion of muscle fiber types. The right or left gastrocnemius muscle was removed thereby causing an overload on the ipsilateral soleus and plantaris muscles. The contralateral limb served as a control. The type II to type I fiber conversion was followed histochemically in the soleus and plantaris muscles for one to six weeks following surgery. Muscle sections were stained for myofibrillar actomyosin ATPase and NADH tetrazolium reductase. The type I population in the soleus muscle was 99.3% six weeks after synergist removal. The plantaris muscle underwent a two fold increase in the percentage of type I fibers after six weeks. Transitional fibers were prominent in the plantaris muscle and reached their peak at 4% (P<0.05) of the total population, four weeks after surgery.This research was funded in part by grants from The Graduate School at Washington State University, and The Society of the Sigma Xi     

An investigation of arterial insufficiency in the rat hindlimb. Correlation of skeletal muscle bloodflow and glucose utilization in vivo.

Muscle bloodflow and the rate of glucose uptake and phosphorylation were measured in vivo in rats 7 days after unilateral femoral artery ligation and section. Bloodflow was determined by using radiolabelled microspheres. At rest, bloodflow to the gastrocnemius, plantaris and soleus muscles of the ligated limb was similar to their respective mean contralateral control values; however, bilateral sciatic nerve stimulation at 1 Hz caused a less pronounced hyperaemic response in the muscles of the ligated limb, being 59, 63 and 49% of their mean control values in the gastrocnemius, plantaris and soleus muscles respectively. The rate of glucose utilization was determined by using the 2-deoxy[3H]glucose method [Ferré, Leturque, Burnol, Penicaud & Girard (1985) Biochem. J. 228, 103-110]. At rest, the rate of glucose uptake and phosphorylation was statistically significantly increased in the gastrocnemius and soleus muscles of the ligated limb, being 126 and 140% of the mean control values respectively. Bilateral sciatic nerve stimulation at 1 Hz caused a 3-5-fold increase in the rate of glucose utilization by the ligated and contralateral control limbs; furthermore, the rate of glucose utilization was significantly increased in the muscles of the ligated limb, being 140, 129 and 207% of their mean control values respectively. For the range of bloodflow to normally perfused skeletal muscle at rest or during isometric contraction determined in the present study, a linear correlation between the rate of glucose utilization and bloodflow can be demonstrated. Applying similar methods of regression analysis to glucose utilization and bloodflow to muscles of the ligated limb reveals a similar linear correlation. However, the rate of glucose utilization at a given bloodflow is increased in muscles of the ligated limb, indicating an adaptation of skeletal muscle to hypoperfusion.     

Myofascial force transmission between the human soleus and gastrocnemius muscles during passive knee motion

The plantarflexors of the lower limb are often assumed to act as independent actuators, but the validity of this assumption is the subject of considerable debate. This study aims to determine the degree to which passive changes in gastrocnemius muscle length, induced by knee motion, affect the tension in the adjacent soleus muscle. A second aim is to quantify the magnitude of myofascial passive force transmission between gastrocnemius and adjacent soleus. Fifteen healthy volunteers participated. Simultaneous ultrasound images of the gastrocnemius and soleus muscles were obtained during passive knee flexion (0-90°), while keeping the ankle angle fixed at either 70° or 115°. Image correlation analysis was used to quantify muscle fascicle lengths in both muscles. The data show that the soleus muscle fascicles elongate significantly during gastrocnemius shortening. The approximate change in passive soleus force as a result of the observed change in fascicle length was estimated and appears to be <5 N, but this estimate is sensitive to the assumed slack length of soleus.