Comparative analysis of the kinematics of hind limb movements in rats during different kinds of locomotion

A comparative analysis of phases of the locomotor cycle and the dynamics of changes in hind limb joint angles during swimming and stepping movements (on a treadmill), involving the fore- and hind limbs to different degrees, were undertaken in rats. Differences in the sequence and degree of changes in joint angles during locomotion of the types investigated were participation of the forelimbs in locomotion was found to be accompanied by more marked forward carrying of the hind limb. Dependence of the swing phase on duration of the cycle was observed and differences were found in the period of protraction of the limb (F period) during swimming and stepping. The role of central spinal processes and influences of peripheral afferents in the formation of different types of locomotion is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 17, No. 2, pp. 189–198, March–April, 1985.     

Rat muscle blood flows during high-speed locomotion

We previously studied blood flow distribution within and among rat muscles as a function of speed from walking (15 m/min) through galloping (75 m/min) on a motor-driven treadmill. The results showed that muscle blood flows continued to increase as a function of speed through 75 m/min. The purpose of the present study was to have rats run up to maximal treadmill speeds to determine if blood flows in the muscles reach a plateau as a function of running speed over the animals' normal range of locomotory speeds. Muscle blood flows were measured with radiolabeled microspheres at 1 min of running at 75, 90, and 105 m/min in male Sprague-Dawley rats. The data indicate that even at these relatively high treadmill speeds there was still no clear evidence of a plateau in blood flow in most of the hindlimb muscles. Flows in most muscles continued to increase as a function of speed. These observed patterns of blood flow vs. running speed may have resulted from the rigorous selection of rats that were capable of performing the high-intensity exercise and thus only be representative of a highly specific population of animals. On the other hand, the data could be interpreted to indicate that the cardiovascular potential during exercise is considerably higher in laboratory rats than has normally been assumed and that inadequate blood flow delivery to the muscles does not serve as a major limitation to their locomotory performance.     

Functional diversification within and between muscle synergists during locomotion

Locomotion arises from the complex and coordinated function of limb muscles. Yet muscle function is dynamic over the course of a single stride and between strides for animals moving at different speeds or on variable terrain. While it is clear that motor unit recruitment can vary between and within muscles, we know little about how work is distributed within and between muscles under in vivo conditions. Here we show that the lateral gastrocnemius (LG) of helmeted guinea fowl (Numida meleagris) performs considerably more work than its synergist, the medial gastrocnemius (MG) and that the proximal region of the MG (pMG) performs more work than the distal region (dMG). Positive work done by the LG was approximately twice that of the proximal MG when the birds walked at 0.5 ms -1, and four times when running at 2.0 m s-1. This is probably due to different moments at the knee, as well as differences in motor unit recruitment. The dMG performed less work than the pMG because its apparent dynamic stiffness was greater, and because it exhibited a greater recruitment of slow-twitch fibres. The greater compliance of the pMG leads to increased stretch of its fascicles at the onset of force, further enhancing force production. Our results demonstrate the capacity for functional diversity between and within muscle synergists, which increases with changes in gait and speed.     

Rat hindlimb muscle blood flow during level and downhill locomotion

Duringeccentrically biased exercise (e.g., downhill locomotion), whole bodyoxygen consumption and blood lactate concentrations are lower thanduring level locomotion. These general systemic measurements indicatethat muscle metabolism is lower during downhill exercise. This studywas designed to test the hypothesis that hindlimb muscle blood flow iscorrespondingly lower during downhill vs. level exercise. Muscle bloodflow (determined by using radioactive microspheres) was measured inrats after 15 min of treadmill exercise at 15 m/min on the level (L,0°) or downhill (D, 17°). Blood flow to ankle extensormuscles was either lower (e.g., white gastrocnemius muscle: D, 9 ± 2; L, 15 ± 1 ml · min¹ · 100 g¹) or not different(e.g., soleus muscle: D, 250 ± 35; L, 230 ± 21 ml · min¹ · 100 g¹) in downhill vs. levelexercise. In contrast, blood flow to ankle flexor muscles was higher(e.g., extensor digitorum longus muscle: D, 53 ± 5; L, 31 ± 6 ml · min¹ · 100 g¹) during downhill vs.level exercise. When individual extensor and flexor muscle flows weresummed, total flow to the leg was lower during downhill exercise (D,3.24 ± 0.08; L, 3.47 ± 0.05 ml/min). These data indicate thatmuscle blood flow and metabolism are lower during eccentrically biasedexercise but are not uniformly reduced in all active muscles; i.e.,flows are equivalent in several ankle extensor muscles and higher inankle flexor muscles.     

Mechanical aspects of legged locomotion control

We review the mechanical components of an approach to motion science that enlists recent progress in neurophysiology, biomechanics, control systems engineering, and non-linear dynamical systems to explore the integration of muscular, skeletal, and neural mechanics that creates effective locomotor behavior. We use rapid arthropod terrestrial locomotion as the model system because of the wealth of experimental data available. With this foundation, we list a set of hypotheses for the control of movement, outline their mathematical underpinning and show how they have inspired the design of the hexapedal robot, RHex.     

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.     

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.     

Fundamental patterns of bilateral muscle activity in human locomotion

Human gait is characterized by smooth, regular and repeating movements but the control system is complex: there are many more actuators (i.e. muscles) than degrees of freedom in the system. Statistical pattern-recognition techniques have been applied to examine muscle activity signals, but these have all concentrated exclusively on unilateral gait. We report here the application of factor analysis to the electromyographic patterns of 16 muscles (eight bilateral pairs) in ten normal subjects. Consistent with our prior work, we have established two factors, named loading response and propulsion, which correspond with important phases in the gait cycle. In addition, we have also discovered a third factor, which we have named the coordinating factor, that maintains the phase shift between the left and right sides. These findings suggest that the central nervous system solves the problem of high dimensionality by generating a few fundamental signals which control the major muscle groups in both legs.     

Delay of muscle vasodilation to changes in work rate (treadmill grade) during locomotion.

Previous studies examining the delay to the onset of vasodilation have primarily focused on the onset of exercise, a setting complicated by the fact that the muscle pump and the vasodilator systems are both activated, making it difficult to attribute changes in blood flow to one or both. The goal here was to determine the delay to the onset of vasodilation after changes in work rate imposed by changes in treadmill grade (work intensity) during locomotion at a steady speed. The rationale was that constant speed would help ensure constant muscle pump activity (contraction frequency) such that vasodilator responses could be examined in isolation. Seven Sprague-Dawley rats underwent three trials each in which treadmill incline was suddenly ( approximately 1 s) elevated from -10 degrees to +10 degrees. The delay to the onset of vasodilation averaged 5.0 +/- 1.8 s, and this delay was not altered by inhibition of nitric oxide synthase. Similar or longer delays were seen during sinusoidal exercise. Thus there is a significant delay before the onset of vasodilation after an increase in work intensity (muscle force) during locomotory exercise at constant speed.     

Mechanical behavior of skeletal muscle during intermittent voluntary isometric contractions in humans

Vøllestad, N. K., I. Sejersted, and E. Saugen. Mechanical behavior of skeletal muscle duringintermittent voluntary isometric contractions in humans.J. Appl. Physiol. 83(5):1557-1565, 1997.Changes in contractile speed and force-fusionproperties were examined during repetitive isometric contractions withthe knee extensors at three different target force levels. Sevenhealthy subjects were studied at target force levels of 30, 45, and60% of their maximal voluntary contraction (MVC) force. Repeated 6-s contractions followed by 4-s rest were continued until exhaustion. Contractile speed was determined for contractions elicited by electrical stimulation at 1-50 Hz given during exercise and a subsequent 27-min recovery period. Contraction time remained unchanged during exercise and recovery, except for an initial rapid shift in thetwitch properties. Half relaxation time(RT_1/2) decreased gradually by 20-40% during exercise at 30 and 45% of MVC. In the recovery period, RT_1/2 values werenot fully restored to preexercise levels. During exercise at 60% MVC,the RT_1/2 decreased for twitches and increased for the 50-Hz stimulation. In the recovery period after60% MVC, RT_1/2 values declinedtoward those seen after the 30 and 45% MVC exercise. The forceoscillation amplitude in unfused tetani relative to the mean forceincreased during exercise at 30 and 45% MVC but remained unalteredduring the 60% MVC exercise. This altered force-fusion was closelyassociated with the changes inRT_1/2. The faster relaxation mayat least partly explain the increased energy cost of contractionreported previously for the same type of exercise.

     

Effects of surface grade on proximal hindlimb muscle strain and activation during rat locomotion.

Sonomicrometry and electromyography were used to determine how surface grade influences strain and activation patterns in the biceps femoris and vastus lateralis of the rat. Muscle activity is generally present during much of stance and is most intense on an incline, intermediate on the level, and lowest on a decline, where the biceps remains inactive except at high speeds. Biceps fascicles shorten during stance, with strains ranging from 0.07-0.30 depending on individual, gait, and grade. Shortening strains vary significantly among grades (P = 0.05) and average 0.21, 0.16, and 0.14 for incline, level, and decline walking, respectively; similar trends are present during trotting and galloping. Vastus fascicles are stretched while active over the first half of stance on all grades, and then typically shorten over the second half of stance. Late-stance shortening is highest during galloping, averaging 0.14, 0.10, and 0.02 in the leading limb on incline, level, and decline surfaces, respectively. Our results suggest that modulation of strain and activation in these proximal limb muscles is important for accommodating different surface grades.     

Mechanical role of expiratory muscle recruitment during eupnea in supine anesthetized dogs

To assess the mechanical role of the expiratory musculature during eupnea, we recorded the electromyographic (EMG) activity of the triangularis sterni, the external oblique, and the transversus abdominis in eight supine lightly anesthetized dogs and have measured the volume generated by the phasic activation of the expiratory muscles. Activation of the expiratory muscles was invariably associated with a decrease in lung volume below the relaxed position of the respiratory system, a volume equal to 41.3 +/- 8.4 ml. This volume represented roughly 20% of tidal volume generated during spontaneous breathing. The fractional expiratory contribution to the tidal volume was unrelated to the size of the animal. Traction on the forelimbs (limb extension), however, tended to enhance the phasic expiratory activation of both the triangularis sterni and the transversus abdominis in the majority of animals. Moreover, after limb extension, the fractional contribution of tidal volume attributed to the phasic activation of the expiratory muscles increased in all but one animal. During spontaneous breathing with the forelimbs extended, roughly 25% of tidal volume was found to be due directly to phasic expiratory muscle contraction. The present observations firmly establish that in supine lightly anesthetized dogs breathing at rest the expiratory component of tidal volume represents a substantial contribution.     

Muscle pump function during locomotion: mechanical coupling of stride frequency and muscle blood flow

We imposed opposing oscillations in treadmill speed and grade on nine rats to test for direct mechanical coupling between stride frequency and hindlimb blood flow. Resting hindlimb blood flow was 15.5 +/- 1.7 ml/min. For 90 s at 7.5 m/min, rats alternated walking at -10 degrees for 10 s and +10 degrees for 10 s. This elicited oscillations in hindlimb blood flow having an amplitude of 4.1 +/- 0.5 ml/min (18% of mean flow) with a delay presumably due to metabolic vasodilation. Similar oscillations in speed (5.5-9.5 m/min) elicited oscillations in hindlimb blood flow (amplitude 3.4 +/- 0.5 ml/min, 15% of mean flow) with less of a delay, possibly due to changes in vasodilation and muscle pump function. We then simultaneously imposed these speed and grade oscillations out of phase (slow uphill, fast downhill). The rationale was that the oscillations in vasodilation evoked by the opposing oscillations in speed and grade would cancel each other, thereby testing the degree to which stride frequency affects hindlimb blood flow directly (i.e., muscle pumping). Opposing oscillations in speed and grade evoked oscillations in hindlimb blood flow having an amplitude of 3.3 +/- 0.6 ml/min (16% of mean flow) with no delay and directly in phase with the changes in speed and stride frequency. The finding that hindlimb blood flow changes directly with speed (when vasodilation caused by changes in speed and grade oppose each other) indicates that there is a direct coupling of stride frequency and hindlimb blood flow (i.e., muscle pumping).     

Neck muscle vibration disrupts steering of locomotion.

Neck muscle vibration was applied to human subjects to assess the influences of neck abnormal proprioceptive input on the organization and execution of gait. Subjects walked blindfolded to a previously seen target, located straight ahead at ~4 m. Vibration was applied on the right side of the neck, both during and before walking. The variables measured were length, duration, and velocity of trajectory; relative and absolute frontal errors at target; and width of walking support base. Vibration applied during locomotion produced an undershoot of target and deviation of gait trajectory toward the side opposite to vibration. Vibration applied before locomotion produced no effect on length of trajectory but slowing of velocity and nonsystematic deviation. When vibration frequency was increased, the amplitude of the nonsystematic deviation increased. Vibration applied during or before stance trials had minor effects on body sway. Vibration before stance had no effect on the position of mean center of foot pressure, whereas vibration during stance displaced it to the side opposite to the vibrated muscle. We suggest that vibration during locomotion reduces length and velocity of trajectory because of a direct action on the locomotor centers and produces trajectory deviation related to its effect on stance. Vibration before locomotion causes a major, nonsystematic deviation from the planned trajectory, possibly connected to a disorientation of the internal references.     

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.