Effect of muscle stimulation intensity on the heterogeneous function of regions within an architecturally complex muscle

2021 ◽  
Author(s):  
Chris Tijs ◽  
Nicolai Konow ◽  
Andrew A. Biewener
Keyword(s):  
Physiological Function ◽  
Fiber Type ◽  
Distal Region ◽  
Proximal Region ◽  
Medial Gastrocnemius ◽  
Optimal Speed ◽  
Type Composition ◽  
Functional Patterns ◽  
Whole Muscle

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.

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
Keyword(s):  
Motor Unit ◽  
Dynamic Stiffness ◽  
Force Production ◽  
Distal Region ◽  
Proximal Region ◽  
Motor Unit Recruitment ◽  
Medial Gastrocnemius ◽  
Numida Meleagris ◽  
Work Done

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.

Fiber-type composition of nine rat muscles. II. Relationship to protein turnover

1989 ◽  
Vol 257 (6) ◽  
pp. E828-E832 ◽  
Author(s):  
P. J. Garlick ◽  
C. A. Maltin ◽  
A. G. Baillie ◽  
M. I. Delday ◽  
D. A. Grubb
Keyword(s):  
Protein Synthesis ◽  
Regression Analysis ◽  
Protein Turnover ◽  
Fiber Type ◽  
Female Rats ◽  
Protein Breakdown ◽  
Fiber Type Composition ◽  
Type Composition ◽  
Age Regression

Rates of protein synthesis in vivo and fiber-type composition were measured in nine limb muscles of female rats at ages ranging from weaning to 1 yr. In all muscles, there was a decline in protein synthesis with increasing age, mostly as a result of a fall in the RNA content. Rates of protein breakdown and growth were determined in six muscles and these also declined with age. Regression analysis of the data for all ages showed that protein synthesis was correlated with the content of slow oxidative fibers but not with the relative proportions of fast glycolytic to fast oxidative glycolytic fibers.

scholarly journals Phase-contrast MRI reveals mechanical behavior of superficial and deep aponeuroses in human medial gastrocnemius during isometric contraction

2008 ◽  
Vol 105 (4) ◽  
pp. 1312-1320 ◽  
Author(s):  
Ryuta Kinugasa ◽  
Dongsuk Shin ◽  
Junichiro Yamauchi ◽  
Chandan Mishra ◽  
John A. Hodgson ◽  
...  
Keyword(s):  
Isometric Contraction ◽  
Phase Contrast ◽  
Muscle Length ◽  
Distal Region ◽  
Voluntary Contraction ◽  
Proximal Region ◽  
Medial Gastrocnemius ◽  
Segment Length ◽  
Cross Sectional ◽  
The Cross

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.

Mapping of movement in the isometrically contracting human soleus muscle reveals details of its structural and functional complexity

2003 ◽  
Vol 95 (5) ◽  
pp. 2128-2133 ◽  
Author(s):  
Taija Finni ◽  
John A. Hodgson ◽  
Alex M. Lai ◽  
V. Reggie Edgerton ◽  
Shantanu Sinha
Keyword(s):  
Soleus Muscle ◽  
Three Dimensional ◽  
Strong Relationship ◽  
Distal Region ◽  
Proximal Region ◽  
Dimensional Structure ◽  
Velocity Mapping ◽  
Precise Knowledge ◽  
Length Changes

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.

scholarly journals In vivo intramuscular fascicle-aponeuroses dynamics of the human medial gastrocnemius during plantarflexion and dorsiflexion of the foot

2009 ◽  
Vol 107 (4) ◽  
pp. 1276-1284 ◽  
Author(s):  
David D. Shin ◽  
John A. Hodgson ◽  
V. Reggie Edgerton ◽  
Shantanu Sinha
Keyword(s):  
Gastrocnemius Muscle ◽  
Imaging Techniques ◽  
High Stress ◽  
Proximal Region ◽  
Pennation Angle ◽  
Medial Gastrocnemius ◽  
Stress Concentrations ◽  
Fascicle Length ◽  
Medial Gastrocnemius Muscle

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.

Surface pH responses of muscles of different fiber-type composition to catecholamines

1983 ◽  
Vol 54 (6) ◽  
pp. 1667-1672 ◽  
Author(s):  
G. J. Kost
Keyword(s):  
Blood Pressure ◽  
Low Dose ◽  
Fiber Type ◽  
Medial Gastrocnemius ◽  
Local Blood Flow ◽  
Epinephrine Infusion ◽  
Surface Ph ◽  
Pentobarbital Sodium ◽  
Type Composition ◽  
Dose Response Effect

Catecholamines were infused intravenously for 45 min into pentobarbital sodium-anesthetized rabbits. Physiologically low-dose epinephrine (0.125 microgram . min-1 . kg-1) decreased medial gastrocnemius (MG) surface pH (SpH) 0.16 +/- 0.03 (SD) (P less than 0.001) to a low of 7.25 +/- 0.11 and soleus (S) SpH 0.09 +/- 0.04 (P less than 0.01) to a low of 7.33 +/- 0.08 without changing blood pressure significantly. Surface temperature measurements suggested a statistically insignificant small increase in local blood flow in both muscles. With 1.25 microgram . min-1 . kg-1 epinephrine, MG SpH decreased 0.22 +/- 0.05 (P less than 0.001) to a low of 7.17 +/- 0.06 and S SpH decreased 0.10 +/- 0.05 (P less than 0.02) to a low of 7.26 +/- 0.04. The MG SpH decrease exceeded the S SpH decrease in each experiment for both epinephrine infusion levels, and the incremental difference was significantly greater (P less than 0.02) with the higher dose, demonstrating a dose-response effect more pronounced for glycolytic compared with oxidative fibers. Norepinephrine infusions of 1.25 and 2.5 micrograms . min-1 . kg-1 did not change SpH of either muscle significantly, despite increases in blood pressure of 10 +/- 3 (P less than 0.002) and 19 +/- 10 mmHg (P less than 0.02), respectively.

Denervation produces different single fiber phenotypes in fast- and slow-twitch hindlimb muscles of the rat

2006 ◽  
Vol 291 (3) ◽  
pp. 518-528 ◽  
Author(s):  
M. F. Patterson ◽  
G. M. M. Stephenson ◽  
D. G. Stephenson
Keyword(s):  
Skeletal Muscles ◽  
Fiber Type ◽  
Fiber Types ◽  
Functional Changes ◽  
Hindlimb Muscles ◽  
Type Composition ◽  
Structural And Functional Properties ◽  
Neural Factors ◽  
Slow Twitch ◽  
Whole Muscle

Using a single, mechanically skinned fiber approach, we tested the hypothesis that denervation (0 to 50 days) of skeletal muscles that do not overlap in fiber type composition [extensor digitorum longus (EDL) and soleus (SOL) muscles of Long-Evans hooded rats] leads to development of different fiber phenotypes. Denervation (50 day) was accompanied by 1) a marked increase in the proportion of hybrid IIB/D fibers (EDL) and I/IIA fibers (SOL) from 30% to >75% in both muscles, and a corresponding decrease in the proportion of pure fibers expressing only one myosin heavy chain (MHC) isoform; 2) complex muscle- and fiber-type specific changes in sarcoplasmic reticulum Ca2+-loading level at physiological pCa ∼7.1, with EDL fibers displaying more consistent changes than SOL fibers; 3) decrease by ∼50% in specific force of all fiber types; 4) decrease in sensitivity to Ca2+, particularly for SOL fibers (by ∼40%); 5) decrease in the maximum steepness of the force-pCa curves, particularly for the hybrid I/IIA SOL fibers (by ∼35%); and 6) increased occurrence of biphasic behavior with respect to Sr2+activation in SOL fibers, indicating the presence of both slow and fast troponin C isoforms. No fiber types common to the two muscles were detected at any time points ( day 7, 21, and 50) after denervation. The results provide strong evidence that not only neural factors, but also the intrinsic properties of a muscle fiber, influence the structural and functional properties of a particular muscle cell and explain important functional changes induced by denervation at both whole muscle and single cell levels.

scholarly journals How does passive lengthening change the architecture of the human medial gastrocnemius muscle?

2017 ◽  
Vol 122 (4) ◽  
pp. 727-738 ◽  
Author(s):  
Bart Bolsterlee ◽  
Arkiev D’Souza ◽  
Simon C. Gandevia ◽  
Robert D. Herbert
Keyword(s):  
Diffusion Tensor ◽  
Muscle Fibers ◽  
Three Dimensional ◽  
Muscle Length ◽  
Muscle Architecture ◽  
Medial Gastrocnemius ◽  
Fascicle Length ◽  
Muscle Belly ◽  
Whole Muscle

There are few comprehensive investigations of the changes in muscle architecture that accompany muscle contraction or change in muscle length in vivo. For this study, we measured changes in the three-dimensional architecture of the human medial gastrocnemius at the whole muscle level, the fascicle level and the fiber level using anatomical MRI and diffusion tensor imaging (DTI). Data were obtained from eight subjects under relaxed conditions at three muscle lengths. At the whole muscle level, a 5.1% increase in muscle belly length resulted in a reduction in both muscle width (mean change −2.5%) and depth (−4.8%). At the fascicle level, muscle architecture measurements obtained at 3,000 locations per muscle showed that for every millimeter increase in muscle-tendon length above the slack length, average fascicle length increased by 0.46 mm, pennation angle decreased by 0.27° (0.17° in the superficial part and 0.37° in the deep part), and fascicle curvature decreased by 0.18 m−1. There was no evidence of systematic variation in architecture along the muscle’s long axis at any muscle length. At the fiber level, analysis of the diffusion signal showed that passive lengthening of the muscle increased diffusion along fibers and decreased diffusion across fibers. Using these measurements across scales, we show that the complex shape changes that muscle fibers, whole muscles, and aponeuroses of the medial gastrocnemius undergo in vivo cannot be captured by simple geometrical models. This justifies the need for more complex models that link microstructural changes in muscle fibers to macroscopic changes in architecture. NEW & NOTEWORTHY Novel MRI and DTI techniques revealed changes in three-dimensional architecture of the human medial gastrocnemius during passive lengthening. Whole muscle belly width and depth decreased when the muscle lengthened. Fascicle length, pennation, and curvature changed uniformly or near uniformly along the muscle during passive lengthening. Diffusion of water molecules in muscle changes in the same direction as fascicle strains.

Acute antioxidant supplementation and skeletal muscle vascular conductance in aged rats: role of exercise and fiber type

2011 ◽  
Vol 300 (4) ◽  
pp. H1536-H1544 ◽  
Author(s):  
Daniel M. Hirai ◽  
Steven W. Copp ◽  
Peter J. Schwagerl ◽  
Mark D. Haub ◽  
David C. Poole ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Fiber Type ◽  
Whole Body ◽  
Aged Rats ◽  
Antioxidant Treatment ◽  
Vascular Conductance ◽  
Fiber Type Composition ◽  
Hindlimb Muscles ◽  
Type Composition

Age-related increases in oxidative stress contribute to impaired skeletal muscle vascular control. However, recent evidence indicates that antioxidant treatment with tempol (4-hydroxy-2,2,6,6-tetramethylpiperidine-1-oxyl) attenuates flow-mediated vasodilation in isolated arterioles from the highly oxidative soleus muscle of aged rats. Whether antioxidant treatment with tempol evokes similar responses in vivo at rest and during exercise in senescent individuals and whether this effect varies based on muscle fiber type composition are unknown. We tested the hypothesis that redox modulation via acute systemic tempol administration decreases vascular conductance (VC) primarily in oxidative hindlimb locomotor muscles at rest and during submaximal whole body exercise (treadmill running at 20 m/min, 5% grade) in aged rats. Eighteen old (25–26 mo) male Fischer 344 x Brown Norway rats were assigned to either rest ( n = 8) or exercise ( n = 10) groups. Regional VC was determined via radiolabeled microspheres before and after intra-arterial administration of tempol (302 μmol/kg). Tempol decreased mean arterial pressure significantly by 9% at rest and 16% during exercise. At rest, similar VC in 26 out of 28 individual hindlimb muscles or muscle parts following tempol administration compared with control resulted in unchanged total hindlimb muscle VC (control: 0.18 ± 0.02; tempol: 0.17 ± 0.05 ml·min−1·100 g−1·mmHg−1; P > 0.05). During exercise, all individual hindlimb muscles or muscle parts irrespective of fiber type composition exhibited either an increase or no change in VC with tempol (i.e., ↑11 and ↔17 muscles or muscle parts), such that total hindlimb VC increased by 25% (control: 0.93 ± 0.04; tempol: 1.15 ± 0.09 ml·min−1·100 g−1·mmHg−1; P ≤ 0.05). These results demonstrate that acute systemic administration of the antioxidant tempol significantly impacts the control of regional vascular tone in vivo presumably via redox modulation and improves skeletal muscle vasodilation independently of fiber type composition during submaximal whole body exercise in aged rats.

Biochemical and physiological changes in overloaded rat fast- and slow-twitch ankle extensors

1985 ◽  
Vol 59 (2) ◽  
pp. 639-646 ◽  
Author(s):  
R. R. Roy ◽  
K. M. Baldwin ◽  
T. P. Martin ◽  
S. P. Chimarusti ◽  
V. R. Edgerton
Keyword(s):  
Fiber Type ◽  
Relaxation Times ◽  
Glycogen Metabolism ◽  
Medial Gastrocnemius ◽  
Cross Sectional ◽  
Muscle Region ◽  
Type Composition ◽  
Contraction Times ◽  
Slow Twitch ◽  
Fast Twitch

The rat soleus (SOL) or medial gastrocnemius (MG) were chronically overloaded by removing their major synergists bilaterally. After 12–14 wks the overloaded SOL (OS) and overloaded MG (OMG) muscles had approximately 50% greater cross-sectional areas (CSA) than the controls. Maximum twitch (Pt) and tetanic (Po) tensions were approximately 46% larger in the OS compared with the normal SOL. The OMG produced 10 and 37% higher Pt and Po, respectively. Specific tension (Po/CSA) was not altered in either group (P greater than 0.05). Contraction times and half-relaxation times were unchanged. Myofibrillar and myosin ATPase specific activities indicated a shift toward that resembling a slower muscle in both the OS and the red portion but not the white portion of the OMG. Generally, markers of glycogen metabolism were reduced (P less than 0.05) in the same muscle areas that showed reduced ATPase activity. These biochemical results were consistent with the apparent histochemical conversion of fibers from fast-twitch, glycolytic----fast-twitch, oxidative-glycolytic----slow-twitch, oxidative types in these muscle areas. These results suggest that overloading either a fast- or slow-twitch plantarflexor results in an increase in muscle mass and maximum tension and in metabolic shifts that generally resemble those observed in a slower muscle. Further, the degree of adaptation appears to be related to the initial fiber type composition of the muscle and/or of the muscle region.

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