Contributions of phase resetting and interlimb coordination to the adaptive control of hindlimb obstacle avoidance during locomotion in rats: a simulation study

Obstacle avoidance during locomotion is essential for safe, smooth locomotion. Physiological studies regarding muscle synergy have shown that the combination of a small number of basic patterns produces the large part of muscle activities during locomotion and the addition of another pattern explains muscle activities for obstacle avoidance. Furthermore, central pattern generators in the spinal cord are thought to manage the timing to produce such basic patterns. In the present study, we investigated sensory-motor coordination for obstacle avoidance by the hindlimbs of the rat using a neuromusculoskeletal model. We constructed the musculoskeletal part of the model based on empirical anatomical data of the rat and the nervous system model based on the aforementioned physiological findings of central pattern generators and muscle synergy. To verify the dynamic simulation by the constructed model, we compared the simulation results with kinematic and electromyographic data measured during actual locomotion in rats. In addition, we incorporated sensory regulation models based on physiological evidence of phase resetting and interlimb coordination and examined their functional roles in stepping over an obstacle during locomotion. Our results show that the phase regulation based on interlimb coordination contributes to stepping over a higher obstacle and that based on phase resetting contributes to quick recovery after stepping over the obstacle. These results suggest the importance of sensory regulation in generating successful obstacle avoidance during locomotion.     

Age effects on rat hindlimb muscle atrophy during suspension unloading.

Disuse can induce numerous adaptive alterations in skeletal muscle. In the present study the effects of hindlimb unloading on muscle mass and biochemical responses were examined and compared in adult (450 g) and juvenile (200 g) rats after 1, 7, or 14 days of whole body suspension. Quantitatively and qualitatively the soleus (S), gastrocnemius (G), plantaris (P), and extensor digitorum longus (EDL) muscles of the hindlimb exhibited a differential sensitivity to suspension and weightlessness unloading in both adults and juveniles. The red slow-twitch soleus exhibited the most pronounced atrophy under both conditions, with juvenile responses being greater than adult. In contrast, the fast-twitch EDL hypertrophied during suspension and atrophied during weightlessness, with no significant difference between adults and juveniles. Determination of biochemical parameters (total protein, RNA, and DNA) indicated a less rapid rate of response in adult muscles. This was corroborated by assessment of muscle alpha-actin mRNA levels, which indicated a rapid (within 1 day) and significant (P less than 0.05) effect in juveniles but not in adults. The results of this investigation indicate 1) a qualitatively similar differential effect of unloading on muscles of adults and juveniles, 2) a quantitatively reduced and less rapid effect of suspension on adult muscles, and 3) a close similarity of adult and juvenile muscle responses during suspension and spaceflight, suggesting that this ground-based model simulates many of the unloading effects of weightlessness.     

Adaptation of rat lateral gastrocnemius muscle motor units during hindlimb unloading

Contractile and fatigue-resistance properties of 71 lateral gastrocnemius muscle (LG) motor units (MU) following 14 days of hindlimb unloading (HU) were compared to those of 60 LG MU from control rats. The MU properties were assessed from isolated and stimulated individual motor axons. The MU were classified using standard criteria (shape of unfused tetani and fatigue resistance). The HU did not affect LG MU composition, but diminished the maximal tetanic tension (Po) of all MU types: P0 was significantly reduced by about 40% for the slow and fast-resistant MU, and by 18% for the fast-fatigable ones. The speed-related properties of fast-resistant MU became more similar to those of slower MU. The fatigue properties of MU were evaluated during a 5-min exercise test, using two fatigue indexes, FI2 and FI5, which expressed the relative capacity of MU to generate tension after 2 and 5 min, respectively. Results showed that 14 days of HU did not change the fatigue sensitivity of the LG MU. However, when F15 was compared to FI2, a greater decrease was observed after HU than in control conditions for the fast-resistant and fast-intermediate MU. It was concluded that a prolonged fatigue test may show changes in metabolic properties of muscle fibres during 14 days of HU. Specific adaptations of LG MU as well as comparisons with those of the soleus muscle under the same conditions are discussed.     

Asymmetric interlimb role-sharing in mechanical power during human sideways locomotion

Sideways movement at a wide variety of speeds is required in daily life and sports. The purpose of this study was to identify the characteristics of asymmetry in power output between lower limbs during sideways gait patterns. Seven healthy men performed steady-state sideways locomotion at various speeds. The mechanical external power of each limb was calculated and decomposed to the lateral and vertical components by the center of mass velocity and ground reaction force. We acquired data from 126 steps of sideways walking at 0.44–1.21 m/s, and from 41 steps of sideways galloping at 1.04–3.00 m/s. The results showed asymmetric power production between the limbs during sideways locomotion. During sideways walking, the trailing limb predominantly produced positive external power and the leading limb produced predominantly negative external power, and these amplitudes increased with step speed. In contrast, during sideways galloping, negative and subsequent positive power production was observed in both limbs. These differences in asymmetric interlimb role-sharing were mainly due to the vertical component. During sideways galloping, the trailing limb absorbs vertical power produced by the leading limb due to the longer flight time. This characteristic of vertical power production in the trailing limb may explain the presence of a double-support phase, which is not observed during forward running, even at high speeds. Our results will help to elucidate the asymmetric movements of the limbs in lateral directions at various speeds.     

Enhancement of hybrid-fiber types in rat soleus muscle after clenbuterol administration during hindlimb unloading

Our objective was to determine the effects of a clenbuterol (CB) treatment orally administered (2 mg per kg) to rats submitted to 14 days of hindlimb unloading (HU). The morphological and the contractile properties as well as the myosin heavy chain isoforms contained in each fiber type were determined in whole soleus muscles. As classically described after HU, a decrease in muscle wet weight and in body mass associated with a loss of muscular force, an evolution of the contractile parameters towards those of a fast muscle type, and the emergence of fast myosin heavy chain isoforms were observed. The CB treatment in the HU rats helped reduce the decrease in 1) muscle and body weights, 2) force and 3) the proportion of slow fibers, without preventing the emergence of fast myosin isoforms. Clenbuterol induced a complex remodelling of the muscle typing promoting the combination of both slow and fast myosin isoforms within one fiber. To conclude, our data demonstrate that CB administration partially counteracts the effects produced by HU, and they allow us to anticipate advances in the treatment of muscular atrophy.     

Ground reaction forces during treadmill running in microgravity

Astronauts perform treadmill exercise during long-duration space missions to counter the harmful effects of microgravity exposure upon bone, muscle, and cardiopulmonary health. When exercising in microgravity, astronauts wear a harness and bungee system that provides forces that maintain attachment to the treadmill. Typical applied forces are less than body weight. The decreased gravity-replacement force could result in differences in ground-reaction force at a given running speed when compared to those achieved in normal gravity, which could influence the adaptive response to the performed 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.     

EMG patterns of rat ankle extensors and flexors during treadmill locomotion and swimming

Intramuscular electromyography (EMG) was used to determine and compare the recruitment patterns of the rat soleus (Sol), tibialis anterior (TA), and a deep and a superficial portion of the medial gastrocnemius (MG) during treadmill locomotion at various speeds and inclines and during swimming. Raw EMG signals for 10-20 step or stroke cycles were rectified, averaged, and processed to determine cycle period (EMG onset of one cycle to EMG onset of the next cycle), EMG burst duration, and integrated area of the rectified burst (IEMG). Mean EMG per burst was calculated as IEMG/burst duration. IEMG/min was calculated as IEMG times the number of bursts (cycles) per minute. Cycle period and burst duration of the extensors decreased hyperbolically, while the TA burst duration was unchanged, with increased treadmill speed. With increased treadmill speed, IEMG was decreased in the Sol and unchanged in the MG and TA, whereas IEMG/min decreased in the Sol and increased in the MG and TA. An elevation in treadmill incline resulted in an increase in the activation levels of the MG but not in the Sol or TA. These data indicate that the additional power required at increased speeds and/or inclines of treadmill locomotion is derived from the recruitment of the fast extensors, e.g., the MG. The mean cycle period during swimming was similar to that observed during the fastest treadmill locomotion. EMG burst durations and amplitudes, however, were higher in the TA, relatively similar in the MG, and lower in the Sol during swimming than treadmill locomotion.(ABSTRACT TRUNCATED AT 250 WORDS)     

Effect of short-term microgravity and long-term hindlimb unloading on rat cardiac mass and function.

The purpose of this study was to test the hypothesis that exposure to short-term microgravity or long-term hindlimb unloading induces cardiac atrophy in male Sprague-Dawley rats. For the microgravity study, rats were subdivided into four groups: preflight (PF, n = 12); flight (Fl, n = 7); flight cage simulation (Sim, n = 6), and vivarium control (Viv, n = 7). Animals in the Fl group were exposed to 7 days of microgravity during the Spacelab 3 mission. Animals in the hindlimb-unloading study were subdivided into three groups: control (Con, n = 20), 7-day hindlimb-unloaded (7HU, n = 10), and 28-day hindlimb-unloaded (28HU, n = 19). Heart mass was unchanged in adult animals exposed to 7 days of actual microgravity (PF 1.33 +/- 0.03 g; Fl 1.32 +/- 0.02 g; Sim 1.28 +/- 0.04 g; Viv 1.35 +/- 0.04 g). Similarly, heart mass was unaltered with hindlimb unloading (Con 1.40 +/- 0.04 g; 7HU 1.35 +/- 0.06 g; 28HU 1.42 +/- 0.03 g). Hindlimb unloading also had no effect on the peak rate of rise in left ventricular pressure, an estimate of myocardial contractility (Con 8,055 +/- 385 mmHg/s; 28HU 8,545 +/- 755 mmHg/s). These data suggest that cardiac atrophy does not occur after short-term exposure to microgravity and that neither short- nor long-term simulated microgravity alters cardiac mass or function.     

An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion

The neuromuscular control of the hindlimb of American alligators (Alligator mississippiensis) walking on a treadmill was analyzed using simultaneous electromyography (EMG) and cineradiography. EMG and kinematic data were integrated with myological information to discern the interplay of muscles mediating hip and knee movement during the high walk. Twelve muscles, subdivided into 23 individual heads, cross the hip joint of Alligator. Activity patterns of 12 heads of 11 hip muscles and one knee muscle were recorded and quantified. An additional five heads from four muscles were recorded in single individuals. During the stance phase, the caudofemoralis longus prevents hip flexion and actively shortens to retract the femur through an arc of 60–80°. At the same time, the adductor femoris 1 and pubo-ischio-tibialis control femoral abduction. The knee is extended 30–40° during stance by contraction of the femoro-tibialis internus. These stance phase muscles often produce discontinuous, periodic EMG signals within their normal burst profile. In late stance and early swing, the ilio-fibularis and the pubo-ischio-tibialis are responsible for flexing the knee. The limb is protracted by the pubo-ischio-femoralis internus 2 and pubo-ischio-femoralis externus 2, which flex the hip. The ilio-femoralis abducts the limb during swing to suspend it above the tread. The role of the ambiens 1, which is active in midswing, is unclear. The ilio-tibialis 2, flexor-tibialis externus and flexor-tibialis internus 2 yield sporadic, low amplitude EMGs; these muscles are recruited at a very low level, if at all, during the slow high walk. Although EMGs do not conclusively delineate muscle function, activity patterns are particularly helpful in elucidating the complex interaction of muscular heads in this system. J. Morphol. 234:197–212, 1997. © 1997 Wiley-Liss, Inc.     

Relationship between myosin heavy chain IId isoform and fibre types in soleus muscle of the rat after hindlimb suspension

The relationship between the myosin heavy chain (HC) IId isoform and histochemically defined fibre types was investigated in the rat soleus muscle after hindlimb suspension. After 4 weeks of suspension, right and left muscles were removed and fibre type composition and total fibre number were examined by histochemical myosin adenosine triphosphatase staining sections. Myosin HC isoforms were analysed by sodium dodecyl sulphate polyacrylamide gel electrophoresis. After the suspension, there was a significant decrease in the percentage of type I fibres and a concomitant increase in that of type IIa fibres. However, the total number of fibres was not affected by suspension. The synthesis of HC IId isoform, which was not found in the control, and the decrease in the ratio of slow type myosin heavy chain isoform (HC I) were observed after suspension. These results would may suggest that the change of fibre type composition was caused by a shift from type I to IIa fibres after suspension. Furthermore, it could be suggested that the synthesis of HC IId isoform occurred during the stage of type shift from type I to IIa fibres.     

The detuning factor in the dynamics of interlimb rhythmic coordination

 Dynamical models of two coupled biological oscillators interpret the detuning term as an arithmetic difference between the uncoupled frequencies, Δω= (ω₁−ω₂). This Δω interpretation of detuning was addressed in four experiments in which human subjects oscillated pendulums in their right and left hands in 1 : 1 frequency locking in antiphase (Experiments 1–3) or inphase (Experiment 4). Differences between the uncoupled frequencies were manipulated through differences in the equivalent simple pendulum lengths, and the effects of this manipulation on the detuning of relative phase from π or 0 and the standard deviation of relative phase SDφ were measured. In Experiment 1, the same values of ω _i were satisfied by several different physical configurations. The experiment confirmed that the detuning term is related strictly to the uncoupled frequencies rather than to other physical characteristics of the oscillators. Experiments 2, 3 and 4 showed, however, that the particular dependency of fixed point drift and SDφ on Δω depends on the particulars of ω₁ and ω₂. With variations in Δω brought about by different ω₁ and ω₂ that always formed a constant ratio, fixed point drift related inversely to Δω, and SDφ varied with Δω in ways that depended on the magnitude of the constant ratio. These outcomes do not conform to expectations from models of coordination dynamics that interpret detuning as (ω₁−ω₂). Received: 18 October 1993/Accepted in revised form: 2 December 1994     

Electromyographic and kinematic studies of tail movements in dogs during treadmill locomotion

Electromyographic (EMG) activities of three tail muscles, the extensor caudae lateralis (ECL), abductor caudae externus (ACE), and flexor caudae longus (FCL), were recorded bilaterally in seven adult dogs during walking, trotting, and galloping on a treadmill. Each dog's movements were recorded with a 16 mm high-speed camera system, and angular movements of the tail were analyzed. During walking and trotting, reciprocal EMG bursts were observed between right and left tail muscles and corresponded with lateral movements of the tail. The tonic discharges that were observed in ECL and FCL seemed to maintain the position of the tail. During galloping, synchronized EMG activity of all tail muscles produced reactive torques to counter those generated by cyclic limb movements and kept the tail in a stable position. These results suggest that tail movements are important in maintaining body balance during locomotion in the dog. © 1993 Wiley-Liss, Inc.     

Regulation of translation factors during hindlimb unloading and denervation of skeletal muscle in rats

In the rat, denervation and hindlimb unloading are two commonly employed models used to study skeletal muscle atrophy. In these models, muscle atrophy is generally produced by a decrease in protein synthesis and an increase in protein degradation. The decrease in protein synthesis has been suggested to occur by an inhibition at the level of protein translation. To better characterize the regulation of protein translation, we investigated the changes that occur in various translation initiation and elongation factors. We demonstrated that both hindlimb unloading and denervation produce alterations in the phosphorylation and/or total amount of the 70-kDa ribosomal S6 kinase, eukaryotic initiation factor 2 alpha-subunit, and eukaryotic elongation factor 2. Our findings indicate that the regulation of these protein translation factors differs between the models of atrophy studied and between the muscles evaluated (e.g., soleus vs. extensor digitorum longus).