In vivo behavior of muscle fascicles and tendinous tissues in human tibialis anterior muscle during twitch contraction

In this study we investigated the time course of length and velocity of muscle fascicles and tendinous tissues (TT) during isometric twitch contraction, and examined how their interaction relates to the time course of external torque and muscle fascicle force generation. From seven males, supra-maximal twitch contractions (singlet) of the tibialis anterior muscle were induced at 30 degrees , 10 degrees and -10 degrees plantar flexed positions. The length and velocity of fascicles and TT were determined from a series of their transverse ultrasound images. The maximal external torque appeared when the shortening velocity of fascicles was zero. The fascicle and TT length, and external torque showed a 10-30 ms delay of each onset, with a significant difference in half relaxation times at -10 degrees . The time course of TT elongation, and fascicle and tendinous velocities did not differ between joint angles. Curvilinear length-force properties, whose slope of quasi-linear part was ranged from -15.0 to -5.9 N/mm for fascicles and 5.4 to 14.3N/mm for TT, and a loop-like pattern of velocity-force properties, in which the mean power was ranged from 0.14 to 0.80 W for fascicles, and 0.14 to 0.81 W for TT were also observed. These results were attributed to the muscle-tendon interaction, depending on the slack and non-linearity of length-force relationship of compliant TT. We conclude that the mechanical interaction between fascicles and TT, are significant determinants of twitch force and time characteristics.     

In vivo fascicle behavior of synergistic muscles in concentric and eccentric plantar flexions in humans.

Ultrasonography was used to directly measure in vivo fascicle behavior of the medial gastrocnemius (MG) and soleus (SOL) muscles while the subjects (n=6 men) performed maximal voluntary concentric and eccentric plantar flexions at 60, 120, 180 and 240 deg/s. Fascicle shortening and lengthening velocities of MG, obtained from fascicle length changes over time, were significantly higher than those of SOL at +/-120, +/-180 and +240 deg/s, possibly reflecting physiological and mechanical differences between these muscles. On the other hand, the effective fascicle shortening and lengthening velocities, defined as the velocities in the longitudinal direction of muscle belly, were not significantly different between MG and SOL. This could be due to difference in fascicle architecture and/or the existence of mechanical linkages between these muscles. Moreover, when the contribution of tendinous tissues to muscle-tendon complex length change was determined from fascicle length, pennation angle, moment arm and joint angle, it accounted for approximately 50% in both concentric and eccentric trials, but showed considerable intra-subject variations. This result quantifiably demonstrates the importance of tendinous tissues in isokinetically controlled joint movements.     

Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo.

Load-strain characteristics of tendinous tissues (Achilles tendon and aponeurosis) were determined in vivo for human medial gastrocnemius (MG) muscle. Seven male subjects exerted isometric plantar flexion torque while the elongation of tendinous tissues of MG was determined from the tendinous movements by using ultrasonography. The maximal strain of the Achilles tendon and aponeurosis, estimated separately from the elongation data, was 5.1 +/- 1.1 and 5.9 +/- 1.6%, respectively. There was no significant difference in strain between the Achilles tendon and aponeurosis. In addition, no significant difference in strain was observed between the proximal and distal regions of the aponeurosis. The results indicate that tendinous tissues of the MG are homogeneously stretched along their lengths by muscle contraction, which has functional implications for the operation of the human MG muscle-tendon unit in vivo.     

Passive knee movement-induced modulation of the soleus H-reflex and alteration in the fascicle length of the medial gastrocnemius muscle in humans

In humans, an inhibitory via Ia afferent pathway from the medial gastrocnemius (MG) to the soleus (SOL) motoneuron pool has been suggested. Herein, we examined the relation between MG fascicle length changes and the SOL H-reflex modulation during passive knee movement. Twelve subjects performed static and passive (5° s^?1) knee movement tasks with the ankle immobilized using an isokinetic dynamometer in sitting posture. The maximal H- and M-waves were measured at four target angles (20°, 40°, 60°, and 80° flexion from full knee extension). The MG fascicles length and velocity were measured using a B-mode ultrasonic apparatus. Results demonstrated that the SOL Hmax/Mmax; i.e., ratio of the maximal H- to M-waves, was attenuated with increasing MG fascicle length in static tasks. The SOL Hmax/Mmax at 20° was significantly attenuated compared with 60° and 80° with increasing MG fascicle length and lengthening velocity in passive knee extension. However, no significant differences in the SOL Hmax/Mmax were found across the target angles in the passive knee flexion task. In conclusion, as muscle spindles increase their discharge with lengthening fascicle velocity, but keep silent when fascicles shorten, our data suggest that lengthening the MG facilitates an inhibitory Ia pathway from MG to SOL, and modulates SOL motoneuron activity during movements.     

Interaction between fascicles and tendinous structures during counter movement jumping investigated in vivo.

Behavior of fascicles and tendinous structures of the m. gastrocnemius medialis (MG) was quantitatively examined during human jumping in vivo. Eight male subjects performed maximal-effort counter movement jumping (CMJ) motions. Kinematic and kinetic data were obtained using a high-speed camera and a force platform. Behavior of fascicles and tendinous structures was determined using ultrasonography and electromyography. Although the muscle-tendon complex (MTC) shortened by only 1.6% during the downward phase of the counter movement, fascicles shortened as much as 10.4%. This shortening of fascicles caused elongation of tendinous structures by 2.2%. Although the MTC remained at almost constant length during the upward-I phase (-250 to -100 ms before toe-off), fascicles shortened by 19.2% of the initial length with an elongation of tendinous structures by 4.4%. The MTC shortened rapidly by 5.3% of the initial length during the upward-II phase (-100 to 0 ms), whereas fascicles shortened slightly during the first half of this phase and contracted in a quasi-isometric manner during the latter half of this phase. These findings implied that elastic energy was stored in tendinous structures throughout the latter half of the downward phase (1.0 J) and upward-I phase (5.6 J), which was thereafter rapidly released during the upward-II phase (3.8 J). It was found that muscle fibers of the MG were not stretched during counter movement; therefore, stretch reflex and potentiation of the contractile component of the MG might not contribute to the work enhancement in CMJ. It was suggested that the interaction between fascicles and tendinous structures was essential in a generation of higher joint power during the late push-off phase. This behavior of the MTC of the MG in CMJ was quite similar to what was observed in squat jumping performed without counter movement.     

The effects of Achilles tendon compliance on triceps surae mechanics and energetics in walking

Achilles tendon (AT) compliance can affect the generation and transmission of triceps surae muscle forces, and thus has important biomechanical consequences for walking performance. However, the uniarticular soleus (SOL) and the biarticular (GAS) function differently during walking, with in vivo evidence suggesting that their associated fascicles and tendinous structures exhibit unique kinematics during walking. Given the strong association between muscle fiber length, velocity and force production, we conjectured that SOL and GAS mechanics and energetic behavior would respond differently to altered AT compliance. To test this, we characterized GAS and SOL muscle and tendon mechanics and energetics due to systematic changes in tendon compliance using musculoskeletal simulations of walking. Increased tendon compliance enlarged GAS and SOL tendon excursions, shortened fiber operation lengths and affected muscle excitation patterns. For both muscles, an optimal tendon compliance (tendon strains of approximately 5% with maximum isometric force) existed that minimized metabolic energy consumption. However, GAS muscle-tendon mechanics and energetics were significantly more sensitive to changes in tendon compliance than were those for SOL. In addition, GAS was not able to return stored tendon energy during push-off as effectively as SOL, particularly for larger values of tendon compliance. These fundamental differences between GAS and SOL sensitivity to altered tendon compliance seem to arise from the biarticular nature of GAS. These insights are potentially important for understanding the functional consequences of altered Achilles tendon compliance due to aging, injury, or disease.     

Changes in human skeletal muscle architecture and function induced by extended spaceflight

The aim of this study was to quantitatively describe the relationships between joint angles and muscle architecture (lengths (L_f) and angles (Θ_f) of fascicles) of human triceps surae [medial (MG) and lateral (LG) gastrocnemius and soleus (SOL) muscles] in vivo for three men-cosmonaut after long-duration spaceflight. Sagittal sonographs of MG, LG, SOL were taken at ankle was positioned at 15° (dorsiflexion), 0° (neutral position), +15°, and +30° (plantarflexion), with the knee at 90° at rest and after a long-duration spaceflight. At each position, longitudinal ultrasonic images of the MG and LG and SOL were obtained while the cosmonauts was relaxed from which fascicle lengths and angles with respect to the aponeuroses were determined. After space flight plantarflexor force declined significantly (26%; p < 0.001). The internal architecture of the GM, and LG, and SOL muscle was significantly altered. In the passive condition, L_f changed from 45, 53, and 39 mm (knee, 0°, ankle, −15°) to 26, 33, and 28 mm (knee, 90° ankle, 30°) for MG, LG, and SOL, respectively. Different lengths and angles of fascicles, and their changes by contraction, might be related to differences in force-producing capabilities of the muscles and elastic characteristics of tendons and aponeuroses. The three heads of the triceps surae muscle substantially differ in architecture, which probably reflects their functional roles. Differences in fiber length and pennation angle that were observed among the muscles and could be associated with differences in force production and in elastic properties of musculo-tendinous complex and aponeuroses.     

Effects of knee joint angle on the fascicle behavior of the gastrocnemius muscle during eccentric plantar flexions

The present study aimed to clarify the effects of knee joint angle on the behavior of the medial gastrocnemius muscle (MG) fascicles during eccentric plantar flexions. Eight male subjects performed maximal eccentric plantar flexions at two knee positions [fully extended (K0) and 90° flexed (K90)]. The eccentric actions were preceded by static plantar flexion at a 30° plantar flexed position and then the ankle joint was forcibly dorsiflexed to 15° of dorsiflexion with an isokinetic dynamometer at 30°/s and 150°/s. Tendon force was calculated by dividing the plantar flexion torque by the estimated moment arm of the Achilles tendon. The MG fascicle length was determined with ultrasonography. The tendon forces during eccentric plantar flexions were influenced by the knee joint angle, but not by the angular velocity. The MG fascicle lengths were elongated as the ankle was dorsiflexed in K0, but in K90 they were almost constant despite the identical range of ankle joint motion. These results suggested that MG fascicle behavior during eccentric actions was markedly affected by the knee joint angle. The difference in the fascicle behavior between K0 and K90 could be attributed to the non-linear force–length relations and/or to the slackness of tendinous tissues.     

Behavior of fascicles and tendinous structures of human gastrocnemius during vertical jumping.

Behavior of fascicles and tendinous structures of human gastrocnemius medialis (MG) was determined by use of ultrasonography in vivo during jumping. Eight male subjects jumped vertically without countermovement (squat jump, SQJ). Simultaneously, kinematics, kinetics, and electromyography from lower leg muscles were recorded during SQJ. During phase I (-350 to -100 ms before toe-off), muscle-tendon complex (MTC) length was almost constant. Fascicles, however, shortened by 26%, and tendinous structures were stretched by 6%, storing elastic energy of 4.9 J during phase I. During phase II (-100 ms to toe-off), although fascicles generated force quasi-isometrically, MTC shortened rapidly by 5.3%, releasing prestored elastic energy with a higher peak positive power than that of fascicles. Also, the compliance of tendinous structures in vivo was somewhat higher than that of external tendon used in the simulation studies. The results demonstrate that the compliance of tendinous structures, together with no yielding of muscle fibers, allows MTC to effectively generate relatively large power at a high joint angular velocity region during the last part of push-off.     

Muscle-tendon interaction and elastic energy usage in human walking.

The present study was designed to explore how the interaction between the fascicles and tendinous tissues is involved in storage and utilization of elastic energy during human walking. Eight male subjects walked with a natural cadence (1.4 +/- 0.1 m/s) on a 10-m-long force plate system. In vivo techniques were employed to record the Achilles tendon force and to scan real-time fascicle lengths for two muscles (medial gastrocnemius and soleus). The results showed that tendinous tissues of both medial gastrocnemius and soleus muscles lengthened slowly throughout the single-stance phase and then recoiled rapidly close to the end of the ground contact. However, the fascicle length changes demonstrated different patterns and amplitudes between two muscles. The medial gastrocnemius fascicles were stretched during the early single-stance phase and then remained isometrically during the late-stance phase. In contrast, the soleus fascicles were lengthened until the end of the single-stance phase. These findings suggest that the elastic recoil takes place not as a spring-like bouncing but as a catapult action in natural human walking. The interaction between the muscle fascicles and tendinous tissues plays an important role in the process of release of elastic energy, although the leg muscles, which are commonly accepted as synergists, do not have similar mechanical behavior of fascicles in this catapult action.     

Changes in contractile properties and neuromuscular propagation evaluated by simultaneous mechanomyogram and electromyogram during experimentally induced hypothermia.

The present study examined, whether or not mechanomyogram (MMG) amplitude and frequency component could reflect the contractile properties of the triceps surae muscles, composed of relatively slow soleus (SOL) and fast medial gastrocnemius (MG), during experimentally induced hypothermia condition. In eight male subjects, lying in prone position, supramaximal single twitch and repetitive electrical stimulations at 10 Hz were applied at the intramuscular temperatures of control (34 degrees C), 15, 20, and 25 degrees C, respectively. The hypothermia induced substantial reduction in muscle contractile properties, e.g. prolonged twitch contraction and half relaxation times, resulted in a highly significant reduction in the fluctuation of force signal during the repetitive stimulations. These changes were almost mirrored by the similar and significant reductions in the MMG amplitude in both SOL and MG. Power spectrum analysis revealed that peak frequency components of MMG and fluctuation of force were almost matched with the applied stimulation frequencies, independent of the temperature condition. These results strongly suggest that MMG analysis could be employed to study muscle contractile properties varying across different physiological conditions.     

Interaction between fascicle and tendinous tissues in short-contact stretch-shortening cycle exercise with varying eccentric intensities.

The interaction between fascicle and tendinous tissues (TT) in short-contact drop jumps (DJ) with three different drop heights [low (Low), optimal (OP), and high (High)] was examined with 11 subjects. The ground reaction force (F(z)) and ankle and knee joint angles were measured together with real-time ultrasonography (fascicle length) and electromyographic activities of the medial gastrocnemius (MG) and vastus lateralis (VL) muscles during the movement. With increasing drop height, the braking force and flight time increased from Low to OP (P < 0.05). In High, the braking force increased but the flight time decreased compared with OP (P < 0.05). During contact of Low and OP conditions, the length of muscle-tendon unit and TT underwent lengthening before shortening in both MG and VL muscles. However, the two muscles differed in the fascicle behaviors. The MG fascicles behaved isometrically or shortened, and the VL fascicles underwent lengthening before shortening during contact. In High, the TT lengthening in both muscles decreased compared with OP (P < 0.05). The rapid stretch occurred in the MG fascicles but not in VL fascicles during the braking phase. The elastic recoil ratio decreased in both muscles with increasing the intensity during DJ. These findings demonstrated that TT underwent lengthening before shortening during DJ. However, the efficacy of elastic recoil decreased with increasing the drop intensity. The effective catapult action in TT can be limited by the drop intensity. In addition, the measured muscles behaved differently during DJ, providing evidence that each muscle may have a specific means of fascicle-TT interaction.     

Intensity- and muscle-specific fascicle behavior during human drop jumps.

The present study was designed to examine fascicle-tendon interaction in the synergistic medial gastrocnemius (MG) and soleus (Sol) muscles during drop jumps (DJ) performed from different drop heights (DH). Eight subjects performed unilateral DJ with maximal rebounds on a sledge apparatus from different DH. During the exercises, fascicle lengths (using ultrasonography) and electromyographic activities were recorded. The results showed that the fascicles of the MG and Sol muscles behaved differently during the contact phase, but the whole muscle-tendon unit and its tendinous tissue lengthened before shortening in both muscles. The Sol fascicles also lengthened before shortening during the ground contact in all conditions. During the braking phase, the Sol activation increased with increasing DH. However, the amplitude of Sol fascicle lengthening was not dependent on DH during the same phase. In the MG muscle, the fascicles primarily shortened during the braking phase in the lower DH condition. However, in the higher DH conditions, the MG fascicles either behaved isometrically or were lengthened during the braking phase. These results suggest that the fascicles of synergistic muscles (MG and Sol) can behave differently during DJ and that, with increasing DH, there may be specific length change patterns of the fascicles of MG but not of Sol.     

The motor units of cat medial gastrocnemius: electrical and mechanical properties as a function of muscle length.

The effects of changing muscle length on the mechanical properties of 89 motor units from adult cat medial gastrocnemius have been studied in eight experiments. Few differences were found between the effects of length on tetanic tension, twitch tension, twitch-tetanus ratio, twitch contraction time, twitch half relaxation time, rate of force development and electrical activity for fast contracting (twitch contraction time less than or equal to 45 msec) and slowly contracting (greater than 45 msec) units. Those differences that did appear did not persist when these two groups were matched by tetanic tension. It is concluded that the biophysical mechanisms responsible for the changes in mechanical and electrical properties with length must be similar for fast and slow twitch units and not related to potential differences in their muscle fiber type. The effects of changing muscle length on the mechanical properties of the eight whole muscles suggest that changes in force output with length are of minor importance during normal movements as the muscle is found to be electrically active over a relatively narrow range of lengths close to the optimum length for tetanus of the whole muscle. The very shortest muscle lengths at which there is only minimal force development are not used in natural movements, while the declining limb of the length tension curve is at muscle lengths beyond the maximum in situ length.     

Fatigue-induced changes in synergistic muscle force do not match tendon elongation

This study aimed to investigate whether fatigue-induced changes in synergistic muscle forces match their tendon elongation. The medial gastrocnemius muscle (MG) was fatigued by repeated electrical stimulation (1 min×5 times: interval 30 s, intensity: 20–30% of maximal voluntary plantar flexion torque) applied at the muscle belly under a partial occlusion of blood vessels. Before and after the MG fatigue task, ramp isometric contractions were performed voluntarily, during which tendon elongations were determined by ultrasonography, along with recordings of the surface EMG activities of MG, the soleus (SOL) and the lateral gastrocnemius (LG) muscles. The tendon elongation of MG and SOL in post-fatigue ramp was similar, although evoked MG forces dropped nearly to zero. In addition, for a given torque output, the tendon elongation of SOL significantly decreased while that of LG did not, although the activation levels of both muscles had increased. Results suggest that the fatigue-induced changes in force of the triceps surae muscles do not match their tendon elongation. These results imply that the tendons of the triceps surae muscles are mechanically coupled even after selective fatigue of a single muscle.     

Motor unit firing patterns of lower leg muscles during isometric plantar flexion with flexed knee joint position

The ankle flexor and extensor muscles are essential for pedal movements associated with car driving. Neuromuscular activation of lower leg muscles is influenced by the posture during a given task, such as the flexed knee joint angle during car driving. This study aimed to investigate the influence of flexion of the knee joint on recruitment threshold-dependent motor unit activity in lower leg muscles during isometric contraction. Twenty healthy participants performed plantar flexor and dorsiflexor isometric ramp contractions at 30 % of the maximal voluntary contraction (MVC) with extended (0°) and flexed (130°) knee joint angles. High-density surface electromyograms were recorded from medial gastrocnemius (MG), soleus (SOL), and tibialis anterior (TA) muscles and decomposed to extract individual motor units. The torque-dependent change (Δpps /Δ%MVC) of the motor unit activity of MG (recruited at 15 %MVC) and SOL (recruited at 5 %MVC) muscles was higher with a flexed compared with an extended knee joint (p < 0.05). The torque-dependent change of TA MU did not different between the knee joint angles. The motor units within certain limited recruitment thresholds recruited to exert plantar flexion torque can be excited to compensate for the loss of MG muscle torque output with a flexed knee joint.     

Spike-triggered average torque and muscle fiber conduction velocity of low-threshold motor units following submaximal endurance contractions.

The motor unit twitch torque is modified by sustained contraction, but the association to changes in muscle fiber electrophysiological properties is not fully known. Thus twitch torque, muscle fiber conduction velocity, and action potential properties of single motor units were assessed in 11 subjects following an isometric submaximal contraction of the tibialis anterior muscle until endurance. The volunteers activated a target motor unit at the minimum discharge rate in eight 3-min-long contractions, three before and five after an isometric contraction at 40% of the maximal torque, sustained until endurance. Multichannel surface electromyogram signals and joint torque were averaged with the target motor unit potential as trigger. Discharge rate (mean +/- SE, 6.6 +/- 0.2 pulses/s) and interpulse interval variability (33.3 +/- 7.0%) were not different in the eight contractions. Peak twitch torque and recruitment threshold increased significantly (93 +/- 29 and 12 +/- 5%, P <0.05) in the contraction immediately after the endurance task with respect to the preendurance values (0.94 +/- 0.26 mN.m and 3.7 +/- 0.5% of the maximal torque), whereas time to peak of the twitch torque did not change (74.4 +/- 10.1 ms). Muscle fiber conduction velocity decreased and action potential duration increased in the contraction after the endurance (6.3 +/- 1.8 and 9.8 +/- 1.8%, respectively, P <0.05; preendurance values, 3.9 +/- 0.2 m/s and 11.1 +/- 0.8 ms), whereas the surface potential peak-to-peak amplitude did not change (27.1 +/- 3.1 microV). There was no significant correlation between the relative changes in muscle fiber conduction velocity or surface potential duration and in peak twitch torque (R2= 0.04 and 0.10, respectively). In conclusion, modifications in peak twitch torque of low-threshold motor units with sustained contraction are mainly determined by mechanisms not related to changes in action potential shape and in its propagation velocity.     

Muscle fiber and tendon length changes in the human vastus lateralis during slow pedaling.

Muscle fascicle lengths of vastus lateralis (VL) muscle were measured in five healthy men during slow pedaling to investigate the interaction between muscle fibers and tendon. Subjects cycled at a pedaling rate of 40 rpm (98 W). During exercise, fascicle lengths changed from 91 +/- 7 (SE) to 127 +/- 5 mm. It was suggested that fascicles were on the descending limb of their force-length relationship. The average shortening velocity of fascicle was greater than that of muscle-tendon complex in the first half of the knee extension phase and was less in the second half. The maximum shortening velocity of fascicle in the knee extension phase was less than that of muscle-tendon complex by 22 +/- 9%. These discrepancies in velocities were mainly caused by the elongation of the tendinous tissue. It was suggested that the elasticity of VL tendinous tissue enabled VL fascicles to develop force at closer length to their optimal length and kept the maximum shortening velocity of VL fascicles low during slow pedaling.     

In vivo determination of fascicle curvature in contracting human skeletal muscles.

Fascicle curvature of human medial gastrocnemius muscle (MG) was determined in vivo by ultrasonography during isometric contractions at three (distal, central, and proximal) locations (n = 7) and at three ankle angles (n = 7). The curvature significantly (P < 0.05) increased from rest to maximum voluntary contraction (MVC) (0.4-5.2 m(-1)). In addition, the curvature at MVC became larger in the order dorsiflexed, neutral, plantar flexed (P < 0.05). Thus both contraction levels and muscle length affected the curvature. Intramuscular differences in neither the curvature nor the fascicle length were found. The direction of curving was consistent along the muscle: fascicles were concave in the proximal side. Fascicle length estimated from the pennation angle and muscle thickness, under the assumption that the fascicle was straight, was underestimated by ~6%. In addition, the curvature was significantly correlated to pennation angle and muscle thickness. These findings are particularly important for understanding the mechanical functions of human skeletal muscle in vivo.     

In vivo behaviour of human muscle architecture and mechanomyographic response using the interpolated twitch technique

This study investigated the origin of curvilinear change in the superimposed mechanomyogram (MMG) amplitude of the human medial gastrocnemius muscle (MG) with increasing contraction intensity. The superimposed twitch amplitude, the superimposed MMG amplitude and the extent of fascicle shortening were measured using ultrasonic images of electrical stimulation during isometric plantar flexions at levels 20%, 40%, 60%, 80%, and 100% of the maximal voluntary contraction (MVC). The superimposed twitch amplitude, the superimposed MMG amplitude and the extent of fascicle shortening decreased with increasing contraction intensity. The superimposed MMG amplitude and the extent of fascicle shortening showed a curvilinear decrease, while the superimposed twitch amplitude showed a linear decrease at levels up to 80% of the MVC. There was a linear relationship between the superimposed MMG amplitude and the extent of fascicle shortening at different contraction intensities. These results indicate that the superimposed MMG amplitude reflects changes in the extent of fascicle shortening at different contraction intensities better than the superimposed twitch amplitude. Our study suggests that the origin of the curvilinear decrease of superimposed MMG amplitude is associated with a curvilinear decrease of the extent of fascicle shortening with increasing contraction intensity in the human MG.