Automatic tracking of medial gastrocnemius fascicle length during human locomotion

During human locomotion lower extremity muscle-tendon units undergo cyclic length changes that were previously assumed to be representative of muscle fascicle length changes. Measurements in cats and humans have since revealed that muscle fascicle length changes can be uncoupled from those of the muscle-tendon unit. Ultrasonography is frequently used to estimate fascicle length changes during human locomotion. Fascicle length analysis requires time consuming manual methods that are prone to human error and experimenter bias. To bypass these limitations, we have developed an automatic fascicle tracking method based on the Lucas-Kanade optical flow algorithm with an affine optic flow extension. The aims of this study were to compare gastrocnemius fascicle length changes during locomotion using the automated and manual approaches and to determine the repeatability of the automated approach. Ultrasound was used to examine gastrocnemius fascicle lengths in eight participants walking at 4, 5, 6, and 7 km/h and jogging at 7 km/h on a treadmill. Ground reaction forces and three dimensional kinematics were recorded simultaneously. The level of agreement between methods and the repeatability of the automated method were quantified using the coefficient of multiple correlation (CMC). Regardless of speed, the level of agreement between methods was high, with overall CMC values of 0.90 ± 0.09 (95% CI: 0.86-0.95). Repeatability of the algorithm was also high, with an overall CMC of 0.88 ± 0.08 (95% CI: 0.79-0.96). The automated fascicle tracking method presented here is a robust, reliable, and time-efficient alternative to the manual analysis of muscle fascicle length during gait.     

Estimation of cat medial gastrocnemius fascicle lengths during dynamic contractions

In typical muscle models, it is often assumed that the contractile element (fascicle) length depends exclusively on the instantaneous muscle-tendon length and the instantaneous muscle force. In order to test whether the instantaneous fascicle length during dynamic contractions can be predicted from muscle-tendon length and force, fascicle lengths, muscle-tendon lengths, and muscle forces were directly measured in cat medial gastrocnemii during isometric and dynamic contractions. Two theoretical muscle models were developed: model A was based on force-time data obtained during the activation phase and model D on force-time data obtained during the deactivation phase of isometric contractions. To test the models, instantaneous fascicle lengths were predicted from muscle-tendon lengths and forces during dynamic contractions that simulated cat locomotion for speeds ranging from 0.4 to 1.6m/s. The theoretically predicted fascicle lengths were compared with the experimentally measured fascicle lengths. It was found that fascicle lengths were not uniquely associated with muscle-tendon lengths and forces; that is, for a given muscle-tendon length and force, fascicle lengths varied depending on the contractile history. Consequently, models A and D differed in fascicle length predictions; model D (maximum average error=8.5%) was considerably better than model A (maximum average error=22.3%). We conclude from this study that it is not possible to predict the exact fascicle lengths from muscle-tendon lengths and forces alone, however, adequate predictions seem possible based on such a model. The relationship between fascicle length and muscle force and muscle-tendon length is complex and highly non-linear, thus, it appears unlikely that accurate fascicle length predictions can be made without some reference contractions in which fascicle length, muscle-tendon length, and force are measured simultaneously.     

The role of the stretch reflex in the gastrocnemius muscle during human locomotion at various speeds.

In the present study, the fascicle length (L(fa)) of the human medial gastrocnemius (MG) muscle was monitored to evaluate possible input from the short-latency stretch reflex (SLR) during the stance phase of running and to examine its timing at various running speeds. Eight subjects ran at 2.0, 3.5, 5.0, and 6.5 m/s. The L(fa) was measured with the high-speed ultrasound fascicle scanning together with kinematics and myoelectrical activities. The amplitudes and onset latency of SLR activities were determined. During ground contact, the sudden MG fascicle stretch occurred during the early contact at all running speeds. This was followed by the fascicle shortening. The timing of fascicle stretch depended on running speed and type of foot contact. In slower speed conditions (2.0, 3.5, 5 m/s), the MG fascicle stretch and the corresponding SLR activities occurred during the middle of the braking phase. In fast-speed running (6.5 m/s), however, the MG fascicle stretch occurred later compared with the lower speed. The corresponding SLR activities occurred significantly later at the end of the braking phase. In addition to the clear demonstration of the different timings of SLR in MG during ground contact of running, the results imply that the role of the MG SLR during the stance phase of running can be different between fast- and slow-speed running conditions.     

Control of ground reaction forces by hindlimb muscles during cat locomotion

It has been proposed that biarticular muscles are primarily responsible for the control of the direction of external forces, as their activation is closely related and highly sensitive to the direction of external forces. This functional role for biarticular muscles has been supported qualitatively by experimental evidence, but has never been tested quantitatively for lack of a mathematical/mechanical formulation of this theory and the difficulty of measuring individual muscle forces during voluntary movements. The purposes of this study were: (1) to define rules for muscular coordination based on the control of external forces; (2) to develop a model of the cat hindlimb that allows for the calculation of the magnitude and direction of the ground reaction forces (GRFs) produced by individual hindlimb muscles; and (3) to test if the coordination of mono- and biarticular cat hindlimb muscles is related to the control of the resultant GRF. We measured the GRF, hindlimb kinematics, selected muscle forces and activations during cat locomotion. Then, the measured muscle forces were used as input to the hindlimb model to compute the muscle-induced GRF. We assume that if activation (and possibly force) increased as the muscle-induced component of GRF approximated the resultant GRF, then that muscle was used by the central nervous system (CNS) to help control the direction of the external GRF. During cat walking, medial gastrocnemius (MG) and plantaris (PL) forces increased with increasing proximity to the GRF, while soleus (SOL) forces and vastus lateralis (VL) activations did not. SOL and VL activation were most strongly related to the vertical and parallel (braking/accelerating) component of the GRF, respectively. We concluded from these results that MG and PL are primarily responsible for the control of the direction of the GRF, while SOL primarily functions as an anti-gravity muscle, and VL as an acceleration/deceleration muscle.     

Correlation of myoelectric activity and muscle force during selected cat treadmill locomotion

The purpose of this investigation was to associate the force produced by the cat medial gastrocnemius (MG) during unrestrained treadmill locomotion with the corresponding myoelectric signals (MES's). An intervention analysis based on the autoregressive-integrated moving average (ARIMA) process was performed on records obtained at treadmill speeds of 0.67 ms-1 and 2.24 ms-1. Results indicate that the pattern of MG myoelectric activity during a single step cycle may be divided into two parts. The primary burst (E1 burst) of activity occurs before foot contact and represents an energy build up which is related to a major part of the MG force monitored at the tendon. During stance, a second burst of activity is depicted by an almost critically damped second order system, and is responsible for the residual tension observed. Thus in vivo forces can be linked to MES's provided that phase differences between electrical and mechanical responses are taken into account.     

Mechanical output of the cat soleus during treadmill locomotion: in vivo vs in situ characteristics

To study the mechanical output of skeletal muscle, four adult cats were trained to run on a treadmill and then implanted under sterile conditions and anesthesia with a force transducer on the soleus tendon and EMG electrodes in the muscle belly. After a two-week recovery period, five consecutive step cycles were filmed at treadmill speeds of 0.8, 1.3 and 2.2 m s-1. Locomotion data in vivo included individual muscle force, length and velocity changes and EMG during each step cycle. Data for an average step cycle at each speed were compared to the force-velocity properties obtained on the same muscle under maximal nerve stimulation and isotonic loading conditions in situ. Results indicate that the force and power generated at a given velocity of shortening during late stance in vivo were greater at the higher speeds of locomotion than the force and power generated at the same shortening velocity in situ. Strain energy stored in the muscle-tendon unit during the yield phase in early stance is felt to be a major contributor to the muscle's enhanced mechanical output during muscle shortening in late stance.     

Force and surface mechanomyogram relationship in cat gastrocnemius.

The aim of this study was to compare the force (F) and the muscle transverse diameter changes during electrical stimulation of the motor nerve. In four cats the exposed motor nerves of the medial gastrocnemius were stimulated as follows: (a) eight separate trials at fixed firing rates (FR) from 5 to 50 Hz (9 s duration, supramaximal amplitude); (b) 5 to 50 Hz linear sweep in 2.5, 5, 7.5 and 10 s (supramaximal amplitude, separate trials); (c) four separate trials at 40 Hz, the motor units (MUs) being orderly recruited in 2.5, 5, 7.5 and 10 s. The muscle surface displacement was detected by a laser distance sensor pointed at the muscle surface. The resulting electrical signal was termed surface mechanomyogram (MMG). In stimulation patterns (a) and (b) the average F and MMG increased with FR. With respect to their values at 50 Hz the amplitude of the unfused signal oscillations at 5 Hz was much larger in MMG than in force. The signal rising phase was always earlier in MMG than in F. In (c) trials, F increased less in the first than in the second half of the recruiting time. MMG had an opposite behaviour. The results indicate that the force and the lateral displacement are not linearly related. The different behaviour of F and MMG, from low to high level of the MUs' pool activation, suggests that the force generation and the muscle dimensional change processes are influenced by different components of the muscle mechanical model.     

Force and surface mechanomyogram frequency responses in cat gastrocnemius

Muscle surface displacement is a mechanical event taking place simultaneously with the tension generation at the tendon. The two phenomena can be studied by the surface mechanomyogram signal (MMG) (produced by a laser distance sensor) and the force signal (from a load cell). The aim of this paper was to provide data on the reliability of the laser detected MMG in muscle mechanics research. To this purpose it was verified if the laser detected MMG was suitable to estimate a frequency response in the cat medial gastrocnemius and its frequency response was compared with the one retrieved by the force signal at the tendon level. The force and MMG from the exposed medial gastrocnemius of four cats were analysed. The frequency response was investigated by sinusoidally changing the number of orderly recruited motor units, in different trials, in the 0.4-6 Hz range. It resulted that it was possible to model the force and MMG frequency response by a critically damped second-order system with two real double poles and a pure time delay. On the average, the poles were at 1.83 Hz (with 22.6 ms delay) and at 2.75 Hz (with 38 ms delay) for force and MMG, respectively. It can be concluded that MMG appears to be a reliable tool to investigate the muscle frequency response during stimulated isometric contraction. Even though not statistically significant. the differences in the second-order system parameters suggest that different components of the muscle mechanical model may specifically affect the force or MMG.     

Tetanic depression in fast motor units of the cat gastrocnemius muscle.

Ability of muscle fibers to generate force is decreased when higher frequency of stimulation of motor units immediately follows lower frequency. This phenomenon called tetanic depression was found in rat medial gastrocnemius. However, it was not clear whether tetanic depression occurred only in rat muscle or it concerns all mammals. This study was conducted on motor units of cat medial gastrocnemius. Analyses were made at three successive trains of stimulation: 30 Hz, 20 and 30 Hz and again 30 Hz (the first pattern) or 40 Hz, 25 and 40 Hz and 40 Hz (the second pattern). In all fast units force generated within the middle tetanus was lower than force generated at the same, but constant frequency of stimulation applied earlier or later. The mean tetanic depression in 30 Hz tetani amounted to 10.9% for fast fatigable (FF) and 15.9% for fast resistant (FR) motor units, whereas in 40 Hz tetani mean values were 5.6% and 7.3% for FF and FR motor units, respectively. In slow motor units tetanic depression was not observed. These results proved the existence of tetanic depression in the feline muscle and indicated that its intensity depends on the fusion of tetanus. It has been concluded, that the tetanic depression is a general property of fast motor units in mammals.     

The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion

The development of the polarity and bilateral asymmetry of the future adult zooid has been traced to their earliest morphological expression in the palleal bud of Botryllus. The account is based upon continued observation of living buds. The polarized antero-posterior and dorso-ventral axes are first expressed by the skewing of a symmetrical, hemispherical bud towards the anterior end of the parental bud. Identification of these axes is reinforced by the development of a loop-like blood circulation, the primary circulation, in the horizontal plane during the enlargement of the skewed hemisphere to form a stalked vesicle. Bilateral asymmetry is first expressed by the asymmetrical expansion of the vesicle stage. The right posterior corner of the vesicle expands further posteriorly and becomes more acute than the left posterior corner. This larger expansion persists throughout the development of the right atrial cavity, which finally expands across the mid-line to partially surround the gut. The bilateral asymmetry, expressed in the expanded vesicle, is reinforced by the development in sequence of a rounded gut rudiment and a pericardial rudiment in positions that would be expected from the asymmetry of the expanded vesicle. The first appearance of the gut rudiment occurs earlier than had been recognized previously. Conflicting accounts of the time and mode of formation of the pericardial rudiment have been clarified. The results of this study are discussed in the context of determination of bud territory, polarity and bilateral asymmetry.     

Low-frequency depression of tension in the cat gastrocnemius muscle after eccentric exercise.

Subjecting a muscle to a series of eccentric contractions in which the contracting muscle is lengthened results in a number of changes in its mechanical properties. These include a fall in isometric tension that is particularly pronounced during low-frequency stimulation, a phenomenon known as low-frequency depression (LFD). Reports of LFD have not taken into account the shift in optimum length for active tension generation to longer muscle lengths that takes place after eccentric contractions. Given the length dependence of the stimulation frequency-tension curve, we tested the hypothesis that the change in this relationship after eccentric exercise is due to the shift in optimum length. We measured LFD by recording tension in response to a linearly increasing rate of stimulation of the nerve to medial gastrocnemius of anesthetized cats, over the range 0-100 pulses per second. Tension responses were measured before and after 50 eccentric contractions consisting of 6-mm stretches starting at 3 mm below optimum length and finishing at 3 mm above it. An index of LFD was derived from the tension responses to ramp stimulation. It was found that LFD after the eccentric contractions was partly, but not entirely, due to changes in the muscle's optimum length. An additional factor was the effect of fatigue. These observations led to the conclusion that the muscle length dependence of LFD was reduced by eccentric contractions. All of this means that after eccentric exercise the tension deficit at low rates of muscle activation is likely to be less severe than first thought.     

Enzymatic responses of cat medial gastrocnemius fibers to chronic inactivity.

The role of neuromuscular activity in maintaining the normal enzyme heterogeneity found in a predominantly fast mixed muscle was studied. Enzymatic profiles of single fibers in the adult cat medial gastrocnemius (MG) were examined after almost complete elimination of neuromuscular activity for 6 mo. Inactivity was achieved by spinal cord isolation (SI), i.e., spinal transection at T12-T13 and L7-S1 combined with bilateral dorsal rhizotomy between the two transection sites. Cross-sectional area and succinate dehydrogenase (SDH) and alpha-glycerophosphate dehydrogenase (GPD) activities were determined in a population of fibers identified in frozen serial cross sections. Each fiber was categorized as light or dark on the basis of its staining characteristics for qualitative myosin adenosinetriphosphatase (ATPase), alkaline preincubation, and its reaction to fast and slow myosin heavy chain (MHC) antibodies. SI resulted in a conversion of nearly all light (approximately 36% in the control) to dark ATPase fibers. Virtually all MG fibers in the SI cats reacted with the fast MHC antibody, whereas very few fibers reacted with slow MHC antibody. On the basis of fiber cross-sectional area, it was estimated that the MG atrophied by approximately 10% after SI. Compared with the mean of the dark and light ATPase fibers in control (weighted by the percent fiber type distribution), mean SDH activity was significantly lower (approximately 70%) and mean GPD activity was significantly higher (approximately 120%) in the SI cats. These data indicate that prolonged electrical silence of a mixed fast hindlimb extensor results in virtually all fibers expressing fast MHC as well as oxidative and glycolytic enzyme profiles normally observed in fast glycolytic fibers.(ABSTRACT TRUNCATED AT 250 WORDS)     

Velocity of ultrasound in active and passive cat medial gastrocnemius muscle.

The lengths and pinnation angles of muscle fibers in the medial gastrocnemius (MG) muscle have recently been measured in freely moving cats [Hoffer et al., Progr. Brain Res. 80, 75-85 (1989); Muscle Afferents and Spinal Control of Movement (1992)] using an ultrasound transit-time (USTT) technique. This method assumed that the velocity of ultrasound through intact muscles was constant, independent of fiber orientation, muscle activity, load, belly shape, or fiber movement. However, the velocity of ultrasound along and across the fibers has been reported to depend on the state of muscle activation in frog muscle experiments in vitro [Hatta et al., J. Physiol. 403, 193-209 (1988)]. In the present study, the assumption of constant velocity of ultrasound in the cat MG muscle was evaluated. In acute experiments, done in situ with intact blood supply, the USTT was measured along and across cat MG muscle fibers in the passive, reflexly activated and tetanically activated states, with and without changes in muscle fiber length, for situations that reproduced the length and force ranges normally used by cats during locomotion. The velocity of ultrasound was found to be independent of the state of activation or motion of the muscle, and independent of the direction of the measurement with respect to the fiber orientation, within a measurement uncertainty less than or equal to 0.2%. These results validate the use of the USTT technique for the measurement of intramuscular dimensions in freely moving animals.     

Vertebral function during tadpole locomotion

Most anuran larvae show large lateral oscillations at both the tip of the tail and the snout while swimming in a straight line. Although the lateral deflections at the snout have long been considered an inefficient aspect of tadpole locomotion, a recent hydrodynamic model suggests that they may in fact help generate thrust. It is not clear though exactly where this bending takes place. The vertebral column is extremely short and seemingly inflexible in anurans, and any axial flexion that might occur there is hidden within the globose body of the tadpole. Here we test the hypothesis that lateral deflections of the snout correlate with bending of the vertebral column within the torso of tadpoles. To quantify vertebral curvature, three sonomicrometry crystals were surgically implanted along the dorsal midline in locations corresponding to the anterior, middle, and posterior region of the presacral vertebral column. Swimming trials were conducted in a flume where synchronized video recordings were collected in dorsal view. Our results confirm that cyclic lateral bending occurs along the vertebral column during swimming and indicate that vertebral curvature is temporally in phase with lateral oscillation of the snout. Lateral oscillation of the snout increased significantly with increasing vertebral curvature. Similarly, tail beat amplitude also increases significantly with increasing vertebral curvature. Our results suggest that cyclic lateral flexion of the vertebral column, activated by the axial muscle within the torso of tadpoles contributes to snout oscillations and the generation of thrust during undulatory swimming in anuran larvae.     

Interspecies differences of motor units properties in the medial gastrocnemius muscle of cat and rat

The purpose of the study was to analyze the interspecies differences of motor unit contractile properties in two most frequently studied mammals: cats and rats. A total sample of 166 motor units (79 in cats and 85 in rats) was investigated in the medial gastrocnemius muscle. Considerable differences were found in composition of the studied muscle. In cats, fast fatigable, fast resistant and slow units formed 68, 18 and 14% of the investigated population, whereas in rats 36, 52 and 12%, respectively. The contraction and relaxation times of motor units in the cat muscle were evidently longer than in the rat and the border values for fast/slow motor units division in these species were 44 and 20 ms, respectively. The mean values of twitch and tetanic forces appeared to be 7-8 times lower in rats, for fast, while 2-5 times for slow motor units. Also variability between the strongest and the weakest units within each type revealed differences 10-60 times in cats, whereas only 3.5-14 times in rats. The summation of twitches into tetanus for fast units was comparable in both species, but for S units was evidently more effective in the cat. In fast motor units' tetanic contractions evident interspecies differences concerned sag appearance and profiles of unfused tetani of FF and FR units. Differences in contractile properties described in the study may depend on the size, number and innervation ratio of motor units in the muscle of cat and rat, as well as their biochemical variability. Differences in composition of motor unit types and uneven mechanisms of force development may reflect biological adaptation to variable behaviour of cats and rats.     

Postural stability of the human mandible during locomotion

Movements of the head and of the mandible relative to the head were measured in human subjects walking and running on a treadmill at various speeds and inclinations. A miniature magnet and piezo-electric accelerometer assembly was mounted on the mandibular incisors, and a Hall-effect sensor along with a second accelerometer mounted on a maxillary incisor along a common vertical axis. Signals from these sensors provided continuous records of vertical head and mandible acceleration, and relative jaw position. Landing on the heel or on the toe in different forms of locomotion was followed by rapid deceleration of the downward movement of the head and slightly less rapid deceleration of the downward movement of the mandible, i.e., the mandible moved downwards relative to the maxilla, then upwards again to near its normal posture within 200 ms. No tooth contact occurred in any forms of gait at any inclination. The movement of the mandible relative to the maxilla depended on the nature and velocity of the locomotion and their effects on head deceleration. The least deceleration and hence mandibular displacement occurred during toe-landing, for example, during "uphill" running. The maximum displacement of the mandible relative to the head was less than 1mm, even at the fastest running speed. The mechanisms that limit the vertical movements of the jaw within such a narrow range are not known, but are likely to include passive soft-tissue visco-elasticity and stretch reflexes in the jaw-closing muscles.