scholarly journals Three-dimensional architecture of the whole human soleus muscle in vivo

PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e4610 ◽  
Author(s):  
Bart Bolsterlee ◽  
Taija Finni ◽  
Arkiev D’Souza ◽  
Junya Eguchi ◽  
Elizabeth C. Clarke ◽  
...  

Background Most data on the architecture of the human soleus muscle have been obtained from cadaveric dissection or two-dimensional ultrasound imaging. We present the first comprehensive, quantitative study on the three-dimensional anatomy of the human soleus muscle in vivo using diffusion tensor imaging (DTI) techniques. Methods We report three-dimensional fascicle lengths, pennation angles, fascicle curvatures, physiological cross-sectional areas and volumes in four compartments of the soleus at ankle joint angles of 69 ± 12° (plantarflexion, short muscle length; average ± SD across subjects) and 108 ± 7° (dorsiflexion, long muscle length) of six healthy young adults. Microdissection and three-dimensional digitisation on two cadaveric muscles corroborated the compartmentalised structure of the soleus, and confirmed the validity of DTI-based muscle fascicle reconstructions. Results The posterior compartments of the soleus comprised 80 ± 5% of the total muscle volume (356 ± 58 cm3). At the short muscle length, the average fascicle length, pennation angle and curvature was 37 ± 8 mm, 31 ± 3° and 17 ± 4 /m, respectively. We did not find differences in fascicle lengths between compartments. However, pennation angles were on average 12° larger (p < 0.01) in the posterior compartments than in the anterior compartments. For every centimetre that the muscle-tendon unit lengthened, fascicle lengths increased by 3.7 ± 0.8 mm, pennation angles decreased by −3.2 ± 0.9° and curvatures decreased by −2.7 ± 0.8 /m. Fascicles in the posterior compartments rotated almost twice as much as in the anterior compartments during passive lengthening. Discussion The homogeneity in fascicle lengths and inhomogeneity in pennation angles of the soleus may indicate a functionally different role for the anterior and posterior compartments. The data and techniques presented here demonstrate how DTI can be used to obtain detailed, quantitative measurements of the anatomy of complex skeletal muscles in living humans.

PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e2260 ◽  
Author(s):  
Brent J. Raiteri ◽  
Andrew G. Cresswell ◽  
Glen A. Lichtwark

Background.Muscles not only shorten during contraction to perform mechanical work, but they also bulge radially because of the isovolumetric constraint on muscle fibres. Muscle bulging may have important implications for muscle performance, however quantifying three-dimensional (3D) muscle shape changes in human muscle is problematic because of difficulties with sustaining contractions for the duration of anin vivoscan. Although two-dimensional ultrasound imaging is useful for measuring local muscle deformations, assumptions must be made about global muscle shape changes, which could lead to errors in fully understanding the mechanical behaviour of muscle and its surrounding connective tissues, such as aponeurosis. Therefore, the aims of this investigation were (a) to determine the intra-session reliability of a novel 3D ultrasound (3DUS) imaging method for measuringin vivohuman muscle and aponeurosis deformations and (b) to examine how contraction intensity influencesin vivohuman muscle and aponeurosis strains during isometric contractions.Methods.Participants (n= 12) were seated in a reclined position with their left knee extended and ankle at 90° and performed isometric dorsiflexion contractions up to 50% of maximal voluntary contraction. 3DUS scans of the tibialis anterior (TA) muscle belly were performed during the contractions and at rest to assess muscle volume, muscle length, muscle cross-sectional area, muscle thickness and width, fascicle length and pennation angle, and central aponeurosis width and length. The 3DUS scan involved synchronous B-mode ultrasound imaging and 3D motion capture of the position and orientation of the ultrasound transducer, while successive cross-sectional slices were captured by sweeping the transducer along the muscle.Results.3DUS was shown to be highly reliable across measures of muscle volume, muscle length, fascicle length and central aponeurosis length (ICC ≥ 0.98, CV < 1%). The TA remained isovolumetric across contraction conditions and progressively shortened along its line of action as contraction intensity increased. This caused the muscle to bulge centrally, predominantly in thickness, while muscle fascicles shortened and pennation angle increased as a function of contraction intensity. This resulted in central aponeurosis strains in both the transverse and longitudinal directions increasing with contraction intensity.Discussion.3DUS is a reliable and viable method for quantifying multidirectional muscle and aponeurosis strains during isometric contractions within the same session. Contracting muscle fibres do work in directions along and orthogonal to the muscle’s line of action and central aponeurosis length and width appear to be a function of muscle fascicle shortening and transverse expansion of the muscle fibres, which is dependent on contraction intensity. How factors other than muscle force change the elastic mechanical behaviour of the aponeurosis requires further investigation.


2017 ◽  
Vol 122 (4) ◽  
pp. 727-738 ◽  
Author(s):  
Bart Bolsterlee ◽  
Arkiev D’Souza ◽  
Simon C. Gandevia ◽  
Robert D. Herbert

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.


1986 ◽  
Vol 250 (3) ◽  
pp. C474-C479 ◽  
Author(s):  
S. S. Segal ◽  
T. P. White ◽  
J. A. Faulkner

Skeletal muscle grafts have a deficit in tension development compared with control muscles, even after accounting for reduced mass and total muscle cross-sectional area. Our purpose was to determine relationships among the architecture, tissue composition, and contractile properties of rat soleus muscle grafts. Data were compared with control soleus muscles obtained from littermates. Female Wistar rats were anesthetized with pentobarbital sodium for grafting of soleus muscles with nerve implant and for dissection of muscles 56 days after grafting. Compared with control values, the maximum specific tension (N/cm2) of grafts was 76%, the interstitial (inulin) space was 135%, and the connective tissue protein concentration was 177%. For grafts, total muscle length and fiber length were 91 and 123% of control values, respectively. The extrapolated shortening velocity at zero load (fiber lengths/s) for grafts was not different from the control value. The deficit in specific tension of grafts is explained by a greater concentration of noncontractile tissue components. Changes in muscle architecture and composition following grafting had little affect on contraction dynamics.


2008 ◽  
Vol 104 (2) ◽  
pp. 469-474 ◽  
Author(s):  
Christopher I. Morse ◽  
Keith Tolfrey ◽  
Jeanette M. Thom ◽  
Vasilios Vassilopoulos ◽  
Constantinos N. Maganaris ◽  
...  

The aim of this study was to assess whether the in vivo specific force and architectural characteristics of the lateral gastrocnemius (GL) muscle of early pubescent boys ( n = 11, age = 10.9 ± 0.3 yr, Tanner stage 2) differed from those of adult men ( n = 12, age = 25.3 ± 4.4 yr). Plantarflexor torque was 55% lower in the boys (77.4 ± 21.4 N·m) compared with the adults (175.6 ± 31.7 N·m, P < 0.01). Physiological cross-sectional area (PCSA), determined in vivo using ultrasonography and MRI, was 52% smaller in the boys ( P < 0.01). No difference was found in pennation angle, or in the ratio of fascicle length ( Lf) to muscle length between the boys and men. Moment arm length was 25% smaller in the boys ( P < 0.01). Antagonist coactivation, assessed using surface EMG on the dorsiflexors, was not different between the boys and men (11.8 ± 6.7% and 13.5 ± 5.8%, respectively). Surprisingly, GL force normalized to PCSA (specific force) was significantly higher (21%) in the boys than in the men (13.1 ± 2.0 vs. 15.9 ± 2.7 N/cm2, P < 0.05). This finding could not be explained by differences in moment arm length, muscle activation, or architecture, and other factors, such as tendinous characteristics and/or changes in moment arm length with contraction, may be held responsible. These observations warrant further investigation.


2007 ◽  
Vol 23 (1) ◽  
pp. 20-41 ◽  
Author(s):  
Melissa R. Lachowitzer ◽  
Anne Ranes ◽  
Gary T. Yamaguchi

In order to create a flexible model of the foot for dynamic musculoskeletal models, anthropometric data combined with geometric information describing the intrinsic musculature are needed. In this study, the left feet of two male and two female cadavers were dissected to expose the intrinsic musculotendon pathways. Three-dimensional coordinates of bony landmarks, tendon origins, insertions, and via points were digitized to submillimeter accuracy. Muscle architectural parameters were also measured, including volume, weight, and pennation angle and sarcomere, fascicle, and free tendon lengths. Optimal muscle fascicle lengths, pennation angles at optimal length, physiological cross-sectional areas (PCSA), and tendon slack lengths were calculated from the directly measured values. Fascicle length and pennation angle varied greatly within each subject. Average fascicle lengths normalized by optimal fascicle length varied between 0.73 and 1.25, with 75% of the formalin-preserved muscles being found in a shortened state. The muscle volume and PCSA also had a large variability within subjects but less variation between subjects. The ratio of tendon slack length to optimal fascicle length was found to vary between 1.05 and 9.56. Using this data, a deformable model of the foot can now be created. It is envisioned that deformable feet will significantly improve


2012 ◽  
Vol 113 (4) ◽  
pp. 517-523 ◽  
Author(s):  
Maoyi Tian ◽  
Robert D. Herbert ◽  
Phu Hoang ◽  
Simon C. Gandevia ◽  
Lynne E. Bilston

The plantarflexors of the lower limb are often assumed to act as independent actuators, but the validity of this assumption is the subject of considerable debate. This study aims to determine the degree to which passive changes in gastrocnemius muscle length, induced by knee motion, affect the tension in the adjacent soleus muscle. A second aim is to quantify the magnitude of myofascial passive force transmission between gastrocnemius and adjacent soleus. Fifteen healthy volunteers participated. Simultaneous ultrasound images of the gastrocnemius and soleus muscles were obtained during passive knee flexion (0–90°), while keeping the ankle angle fixed at either 70° or 115°. Image correlation analysis was used to quantify muscle fascicle lengths in both muscles. The data show that the soleus muscle fascicles elongate significantly during gastrocnemius shortening. The approximate change in passive soleus force as a result of the observed change in fascicle length was estimated and appears to be <5 N, but this estimate is sensitive to the assumed slack length of soleus.


2017 ◽  
Vol 117 (4) ◽  
pp. 1489-1498 ◽  
Author(s):  
James Day ◽  
Leah R. Bent ◽  
Ingvars Birznieks ◽  
Vaughan G. Macefield ◽  
Andrew G. Cresswell

Muscle spindles provide exquisitely sensitive proprioceptive information regarding joint position and movement. Through passively driven length changes in the muscle-tendon unit (MTU), muscle spindles detect joint rotations because of their in-parallel mechanical linkage to muscle fascicles. In human microneurography studies, muscle fascicles are assumed to follow the MTU and, as such, fascicle length is not measured in such studies. However, under certain mechanical conditions, compliant structures can act to decouple the fascicles, and, therefore, the spindles, from the MTU. Such decoupling may reduce the fidelity by which muscle spindles encode joint position and movement. The aim of the present study was to measure, for the first time, both the changes in firing of single muscle spindle afferents and changes in muscle fascicle length in vivo from the tibialis anterior muscle (TA) during passive rotations about the ankle. Unitary recordings were made from 15 muscle spindle afferents supplying TA via a microelectrode inserted into the common peroneal nerve. Ultrasonography was used to measure the length of an individual fascicle of TA. We saw a strong correlation between fascicle length and firing rate during passive ankle rotations of varying rates (0.1–0.5 Hz) and amplitudes (1–9°). In particular, we saw responses observed at relatively small changes in muscle length that highlight the sensitivity of the TA muscle to small length changes. This study is the first to measure spindle firing and fascicle dynamics in vivo and provides an experimental basis for further understanding the link between fascicle length, MTU length, and spindle firing patterns. NEW & NOTEWORTHY Muscle spindles are exquisitely sensitive to changes in muscle length, but recordings from human muscle spindle afferents are usually correlated with joint angle rather than muscle fascicle length. In this study, we monitored both muscle fascicle length and spindle firing from the human tibialis anterior muscle in vivo. Our findings are the first to measure these signals in vivo and provide an experimental basis for exploring this link further.


1986 ◽  
Vol 61 (1) ◽  
pp. 173-179 ◽  
Author(s):  
P. Loughna ◽  
G. Goldspink ◽  
D. F. Goldspink

A state of hypokinesia and hypodynamia has been induced in the hindlimb muscles of the rat (100 g) using a suspension model. The ensuing muscle atrophy was assessed by reference to muscles in fully mobile control animals, which were either fed ad libitum or fed the same lower food intake of the suspended animals. Over a total of 7 days of suspension the slow-twitch postural soleus muscle underwent a much greater atrophy than the fast-twitch phasic extensor digitorum longus. Changes with respect to the position of the suspended foot, and hence muscle length, necessitate caution in comparing the extent of the atrophy between different muscle types. After 3 days of inactivity the atrophy of the soleus muscle was explained by a 21% decrease in the fractional rate of synthesis (measured in vivo) and a 100% increase in the rate of protein breakdown. The reduction in the synthetic rate was associated with a net loss (23%) of RNA and hence muscle ribosomes. In contrast when this inactive soleus muscle was permanently stretched the RNA content (44%) and protein synthetic rate increased (59%) markedly above control values. Although protein breakdown remained elevated in this stretched muscle, the extent of the atrophy in response to hypokinesia and hypodynamia was greatly reduced.


2015 ◽  
Vol 282 (1819) ◽  
pp. 20151908 ◽  
Author(s):  
François Hug ◽  
Clément Goupille ◽  
Daniel Baum ◽  
Brent J. Raiteri ◽  
Paul W. Hodges ◽  
...  

The force produced by a muscle depends on both the neural drive it receives and several biomechanical factors. When multiple muscles act on a single joint, the nature of the relationship between the neural drive and force-generating capacity of the synergistic muscles is largely unknown. This study aimed to determine the relationship between the ratio of neural drive and the ratio of muscle force-generating capacity between two synergist muscles (vastus lateralis (VL) and vastus medialis (VM)) in humans. Twenty-one participants performed isometric knee extensions at 20 and 50% of maximal voluntary contractions (MVC). Myoelectric activity (surface electromyography (EMG)) provided an index of neural drive. Physiological cross-sectional area (PCSA) was estimated from measurements of muscle volume (magnetic resonance imaging) and muscle fascicle length (three-dimensional ultrasound imaging) to represent the muscles' force-generating capacities. Neither PCSA nor neural drive was balanced between VL and VM. There was a large ( r = 0.68) and moderate ( r = 0.43) correlation between the ratio of VL/VM EMG amplitude and the ratio of VL/VM PCSA at 20 and 50% of MVC, respectively. This study provides evidence that neural drive is biased by muscle force-generating capacity, the greater the force-generating capacity of VL compared with VM, the stronger bias of drive to the VL.


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