scholarly journals Functional diversification within and between muscle synergists during locomotion

2007 ◽  
Vol 4 (1) ◽  
pp. 41-44 ◽  
Author(s):  
Timothy E Higham ◽  
Andrew A Biewener ◽  
James M Wakeling

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 m s −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.

Author(s):  
Chris Tijs ◽  
Nicolai Konow ◽  
Andrew A. Biewener

Skeletal muscle has fiber architectures ranging from simple to complex, alongside variation in fiber-type and neuro-anatomical compartmentalization. However, the functional implications of muscle subdivision into discrete functional units remain poorly understood. The rat medial gastrocnemius has well-characterized regions with distinct architectures and fiber type composition. Here, force-length and force-velocity contractions were performed for two stimulation intensities (supramaximal and submaximal) and for three structural units (whole muscle belly, proximal region and distal region) to assess the effect of muscle compartmentalization on contractile force-length-velocity relations and optimal speed for power production. Additionally, fiber strain, fiber rotation, pennation, and architectural gearing were quantified. Our results suggest that the proximal and distal muscle regions have fundamentally different physiological function. During supramaximal activation, the proximal region has shorter (8.4±0.8mm vs 10.9±0.7mm) fibers and steeper (28.7±11.0° vs 19.6±6.3°) fiber angles at optimum length, and operates over a larger (17.9 ± 3.8% vs 12.6 ± 2.7%) range of its force-length curve. The proximal region also exhibits larger changes in pennation angle (5.6 ± 2.2°/mm vs 2.4 ± 1.5°/mm muscle shortening) and architectural gearing (1.82 ± 0.53 vs 1.25 ± 0.24); whereas, the distal region exhibits greater peak shortening speed (96.0mm/s vs 81.3mm/s) and 18-27% greater optimal speed. Overall, similar patterns were observed during submaximal activation. These regional differences in physiological function with respect to the whole muscle highlight how variation in motor recruitment could fundamentally shift regional functional patterns within a single muscle, which likely has important implications for whole muscle force and work output in vivo.


2002 ◽  
Vol 205 (3) ◽  
pp. 359-369 ◽  
Author(s):  
James M. Wakeling ◽  
Motoshi Kaya ◽  
Genevieve K. Temple ◽  
Ian A. Johnston ◽  
Walter Herzog

SUMMARY Motor units are the functional units of muscle contraction in vertebrates. Each motor unit comprises muscle fibres of a particular fibre type and can be considered as fast or slow depending on its fibre-type composition. Motor units are typically recruited in a set order, from slow to fast, in response to the force requirements from the muscle. The anatomical separation of fast and slow muscle in fish permits direct recordings from these two fibre types. The frequency spectra from different slow and fast myotomal muscles were measured in the rainbow trout Oncorhynchus mykiss. These two muscle fibre types generated distinct low and high myoelectric frequency bands. The cat paw-shake is an activity that recruits mainly fast muscle. This study showed that the myoelectric signal from the medial gastrocnemius of the cat was concentrated in a high frequency band during paw-shake behaviour. During slow walking, the slow motor units of the medial gastrocnemius are also recruited, and this appeared as increased muscle activity within a low frequency band. Therefore, high and low frequency bands could be distinguished in the myoelectric signals from the cat medial gastrocnemius and probably corresponded, respectively, to fast and slow motor unit recruitment. Myoelectric signals are resolved into time/frequency space using wavelets to demonstrate how patterns of motor unit recruitment can be determined for a range of locomotor activities.


2008 ◽  
Vol 105 (4) ◽  
pp. 1312-1320 ◽  
Author(s):  
Ryuta Kinugasa ◽  
Dongsuk Shin ◽  
Junichiro Yamauchi ◽  
Chandan Mishra ◽  
John A. Hodgson ◽  
...  

The behavior of the entire medial gastrocnemius (MG) superficial and deep aponeurosis structure was investigated with velocity-encoded phase-contrast, spin-tag, and three-dimensional morphometric magnetic resonance imaging. The displacements and strain of both these aponeuroses, muscle length, and the cross-sectional segment length of the deep aponeurosis were measured during isometric plantarflexion at 20% and 40% of maximal voluntary contraction (MVC). The length of the entire MG shortened during 20% and 40% MVC. All regions of interest in both aponeuroses moved proximally. Positive strain (lengthening) occurred in both ends of the deep aponeurosis and in the proximal region of the superficial aponeurosis. In contrast, negative strain (shortening) was observed in the middle region of the deep aponeurosis and in the distal region of the superficial aponeurosis. Consistent with this shortening of the deep aponeurosis length along the proximal-distal axis was expansion of the aponeuroses in the medial-lateral and anterior-posterior directions in the cross-sectional plane. It is concluded that at low to moderate force levels of isometric contraction, regional differences in strain occur along the proximal-distal axis of both aponeuroses, and some regions of both aponeuroses shorten.


2006 ◽  
Vol 3 (9) ◽  
pp. 533-544 ◽  
Author(s):  
James M Wakeling ◽  
Katrin Uehli ◽  
Antra I Rozitis

This study investigates the motor unit recruitment patterns between and within muscles of the triceps surae during cycling on a stationary ergometer at a range of pedal speeds and resistances. Muscle activity was measured from the soleus (SOL), medial gastrocnemius (MG) and lateral gastrocnemius (LG) using surface electromyography (EMG) and quantified using wavelet and principal component analysis. Muscle fascicle strain rates were quantified using ultrasonography, and the muscle–tendon unit lengths were calculated from the segmental kinematics. The EMG intensities showed that the body uses the SOL relatively more for the higher-force, lower-velocity contractions than the MG and LG. The EMG spectra showed a shift to higher frequencies at faster muscle fascicle strain rates for MG: these shifts were independent of the level of muscle activity, the locomotor load and the muscle fascicle strain. These results indicated that a selective recruitment of the faster motor units occurred within the MG muscle in response to the increasing muscle fascicle strain rates. This preferential recruitment of the faster fibres for the faster tasks indicates that in some circumstances motor unit recruitment during locomotion can match the contractile properties of the muscle fibres to the mechanical demands of the contraction.


1996 ◽  
Vol 75 (1) ◽  
pp. 26-37 ◽  
Author(s):  
K. E. Tansey ◽  
B. R. Botterman

1. The recruitment order of 64 pairs of motor units, comprising 21 type-identified units, was studied during centrally evoked muscle contractions of the cat medial gastrocnemius (MG) muscle in an unanesthetized, high decerebrate preparation. Motor units were functionally isolated within the MG nerve by intra-axonal (or intramyelin) penetration with conventional glass microelectrodes. 2. Graded stimulation of the mesencephalic locomotor region (MLR) was used to evoke smoothly graded contractions, which under favorable conditions was estimated to reach 40% of maximum tetanic tension of the MG muscle. With this method of activation, 100% of slow twitch (type S) units, 95% of fast twitch, fatigue-resistant (type FR) units, 86% of fast twitch, fatigue-intermediate (type FI) units, and 49% of fast twitch, fatigable (type FF) units studied were recruited. 3. Motoneuron size as estimated by axonal conduction velocity (CV) was correlated with muscle-unit size as estimated by maximum tetanic tension (Po). Although the correlation between these properties was significant among type S and FR units, no significant correlation was found for these properties among type FI and FF units. 4. Motor-unit recruitment was ordered by physiological type (S > F, 100% of pairs; S > FR > FI > FF, 93% of pairs). Although none of the motor-unit properties studied predicted recruitment order perfectly, motor-unit recruitment was found to proceed by increasing Po (89% of pairs), decreasing contraction time (79% of pairs), decreasing fatigue index (80% of pairs), and increasing CV (76% of pairs). These percentages were significantly different from random (i.e., 50%). Statistically, all four motor-unit properties were equivalent in predicting recruitment order. These results are similar to those reported by other investigators for motor-unit recruitment order evoked from other supraspinal centers, as well as from peripheral sites. 5. When, however, motor-unit recruitment within pairs of motor units containing two fast-twitch (type F) units was examined, Po was a significantly better predictor of recruitment order than CV (85% vs. 52% of pairs). One explanation for this observation is that the correlation between Po and CV is high among type S, type FR units, and possibly among the lower-tension type FF units, but not among the remaining higher-tension type FF units. 6. The reproducibility of recruitment order in multiple contractions was investigated in 16 motor-unit pairs. Recruitment order was found to be variable in only three motor-unit pairs, all of which contained units of similar physiological type and recruitment threshold. 7. Analysis of recruitment order by pair-wise testing confirms the general conclusion reached in human studies that the muscle force level at recruitment for a motor unit is highly correlated with its strength. As an additional confirmation, the whole-muscle force level at recruitment for 41 units was measured in a series of contractions in which the rate of rise of muscle tension was limited to rates < 1,000 g/s. For these contractions, a significant correlation was found between muscle tension at recruitment and motor-unit Po.


2003 ◽  
Vol 95 (5) ◽  
pp. 2128-2133 ◽  
Author(s):  
Taija Finni ◽  
John A. Hodgson ◽  
Alex M. Lai ◽  
V. Reggie Edgerton ◽  
Shantanu Sinha

It is becoming increasingly apparent that precise knowledge of the anatomic features of muscle, aponeurosis, and tendons is necessary for understanding how a muscle-tendon complex generates force and accomplishes length changes. This report presents both anatomic and functional data from the human soleus muscle acquired by using magnetic resonance imaging. The results show a strong relationship between the complex three-dimensional structure of the muscle-tendon system and the intramuscular distribution of tissue velocities during in vivo isometric contractions. The proximal region of the muscle is unipennate, whereas the midregion has a radially bipennate hemicylindrical structure, and the distal region is quadripennate. Tissue velocity mapping shows that the highest velocity regions overlay the aponeuroses connected to the Achilles tendon. These are located on the anterior and posterior surfaces of the muscle. The lowest velocities overlay the aponeuroses connected to the origin of the muscle and are generally located intramuscularly.


2009 ◽  
Vol 107 (4) ◽  
pp. 1276-1284 ◽  
Author(s):  
David D. Shin ◽  
John A. Hodgson ◽  
V. Reggie Edgerton ◽  
Shantanu Sinha

Velocity-encoded phase-contrast magnetic resonance (MR) imaging techniques and a computer-controlled MR-compatible foot pedal device were used to investigate the medial gastrocnemius muscle and aponeurosis deformations during passive and active eccentric movements of the plantarflexors. Intrafascicular strain, measured as the ratio of strain in the fascicle segment at its insertion to strain at its origin, was nonuniform along the proximodistal axis of the muscle ( P < 0.01), progressively increasing from the proximal to distal direction. The high intrafascicular strain regions appeared to correlate with the muscle regions that are likely to encounter high stress concentrations, i.e., the regions where the muscle physiological cross section decreases close to the tendons. The architectural gear ratio, i.e., the mechanical amplification ratio of fascicle length displacement to that of tendon/aponeuroses in a pennate muscle, also exhibited significant regional differences, with the highest ratios in the proximal region of the muscle accompanied by a higher initial pennation angle and a larger range of fascicular rotation about the origin. Values close to unity in the distal region of the muscle suggest that the aponeurosis separation may decrease in this region. Fascicle length and pennation angle changes were significantly influenced by force generation in the muscle, probably due to a shortening of the loaded muscle fibers relative to a passive condition. Overall, our data illustrate significant proximodistal intramuscular heterogeneity as supported by a regionally variable end-to-end strain ratio of fascicles and angle changes in the medial gastrocnemius muscle during passive and active ankle movements. These observations emphasize the need to reassess current conceptual models of muscle-tendon mechanics.


2021 ◽  
Vol 18 (174) ◽  
pp. 20200765
Author(s):  
Adrian K. M. Lai ◽  
Taylor J. M. Dick ◽  
Andrew A. Biewener ◽  
James M. Wakeling

The nervous system is faced with numerous strategies for recruiting a large number of motor units within and among muscle synergists to produce and control body movement. This is challenging, considering multiple combinations of motor unit recruitment may result in the same movement. Yet vertebrates are capable of performing a wide range of movement tasks with different mechanical demands. In this study, we used an experimental human cycling paradigm and musculoskeletal simulations to test the theory that a strategy of prioritizing the minimization of the metabolic cost of muscle contraction, which improves mechanical efficiency, governs the recruitment of motor units within a muscle and the coordination among synergist muscles within the limb. Our results support our hypothesis, for which measured muscle activity and model-predicted muscle forces in soleus—the slower but stronger ankle plantarflexor—is favoured over the weaker but faster medial gastrocnemius (MG) to produce plantarflexor force to meet increased load demands. However, for faster-contracting speeds induced by faster-pedalling cadence, the faster MG is favoured. Similar recruitment patterns were observed for the slow and fast fibres within each muscle. By contrast, a commonly used modelling strategy that minimizes muscle excitations failed to predict force sharing and known physiological recruitment strategies, such as orderly motor unit recruitment. Our findings illustrate that this common strategy for recruiting motor units within muscles and coordination between muscles can explain the control of the plantarflexor muscles across a range of mechanical demands.


1996 ◽  
Vol 75 (6) ◽  
pp. 2243-2254 ◽  
Author(s):  
C. J. DeRuiter ◽  
A. De Haan ◽  
A. J. Sargeant

1. The effect of muscle unit (MU) localization on physiological properties was investigated within the fast-twitch fatigue-resistant (FR) and fast-fatigable (FF) MU populations of rat medial gastrocnemius (MG) muscle. Single MG MUs were functionally isolated by microdissection of the ventral roots. FR and FF MU properties of the most proximal and distal muscle compartments were compared. The most proximal and distal compartment are subvolumes of the MG innervated by the most proximal and distal primary nerve branch, respectively. A subsample of the isolated units was glycogen depleted and muscle cross sections were stained for glycogen and myosin-adenosinetriphosphatase. 2. It was shown that proximal FF and FR units reached optimum length for force production at shorter muscle lengths compared with the distal FR and FF units. 3. The fast MUs of the proximal compartment had small territories that were located close to and/or within the mixed region (containing type I, IIA, IIX, and IIB fibers) of the muscle. The fast MUs of the distal compartment had greater territories that were located in the more superficial muscle part (containing only type IIX and IIB fibers) and in some cases spanned the entire area of the distal muscle compartment. 4. FR and FF MUs consisted of muscle fibers identified histochemically as type IIX and IIB, respectively. 5. Within each of the FR and FF MU populations, MUs that were located in the most proximal muscle compartment were more resistant to fatigue compared with the units located in the most distal compartment. 6. Cross-sectional fiber areas were smaller for the proximal FR and FF fibers, but specific force did not differ among units. Consequently, when account was taken of the innervation ratio, the proximal FR and FF units produced less force than distal units of the same type. Tetanic forces were 87 +/- 27 (SD) mN (proximal FR), 154 +/- 53 (SD) mN (distal FR), 142 +/- 25 (SD) mN (proximal FF), and 229 +/- 86 (SD) mN (distal FF). 7. The present findings suggest that with increasing demand placed on rat MG during in vivo locomotion, recruitment is likely to proceed from proximal to distal muscle parts within the FR and FF MU populations.


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