Length-force characteristics of in vivo human muscle reflected by supersonic shear imaging

Recently, an ultrasound-based elastography technique has been used to measure stiffness (shear modulus) of an active human muscle along the axis of contraction. Using this technique, we explored 1) whether muscle shear modulus, like muscle force, is length dependent; and 2) whether the length dependence of muscle shear modulus is consistent between electrically elicited and voluntary contractions. From nine healthy participants, ankle joint torque and shear modulus of the tibialis anterior muscle were measured at five different ankle joint angles during tetanic contractions and during maximal voluntary contractions. Fascicle length, pennation angle, and tendon moment arm length of the tetanized tibialis anterior calculated from ultrasound images were used to reveal the length-dependent changes in muscle force and shear modulus. Over the range of joint angles examined, both force and shear modulus of the tetanized muscle increased with increasing fascicle length. Regression analysis of normalized data revealed a significant linear relationship between force and shear modulus ( R2 = 0.52, n = 45, P < 0.001). Although the length dependence of shear modulus was consistent, irrespective of contraction mode, the slope of length-shear modulus relationship was steeper during maximal voluntary contractions than during tetanic contractions. These results provide novel evidence that length-force relationship, one of the most fundamental characteristics of muscle, can be inferred from in vivo imaging of shear modulus in the tibialis anterior muscle. Furthermore, the estimation of length-force relationship may be applicable to voluntary contractions in which neural and mechanical interactions of multiple muscles are involved.

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Muscle spindles in human tibialis anterior encode muscle fascicle length changes

Journal of Neurophysiology ◽

10.1152/jn.00374.2016 ◽

2017 ◽

Vol 117 (4) ◽

pp. 1489-1498 ◽

Cited By ~ 19

Author(s):

James Day ◽

Leah R. Bent ◽

Ingvars Birznieks ◽

Vaughan G. Macefield ◽

Andrew G. Cresswell

Keyword(s):

Muscle Spindle ◽

Tibialis Anterior ◽

Tibialis Anterior Muscle ◽

Muscle Length ◽

Muscle Spindles ◽

Muscle Spindle Afferents ◽

Fascicle Length ◽

Muscle Fascicle ◽

Length Changes

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.

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Microendoscopy reveals positive correlation in multiscale length changes and variable sarcomere lengths across different regions of human muscle

Journal of Applied Physiology ◽

10.1152/japplphysiol.00480.2018 ◽

2018 ◽

Vol 125 (6) ◽

pp. 1812-1820 ◽

Cited By ~ 18

Author(s):

Glen A. Lichtwark ◽

Dominic J. Farris ◽

Xuefeng Chen ◽

Paul W. Hodges ◽

Scott L. Delp

Keyword(s):

Tibialis Anterior ◽

Sarcomere Length ◽

Length Change ◽

Human Muscle ◽

Fascicle Length ◽

Needle Probe ◽

Distal Location ◽

Length Changes ◽

Sarcomere Number

Sarcomere length is a key physiological parameter that affects muscle force output; however, our understanding of the scaling of human muscle from sarcomere to whole muscle is based primarily on cadaveric data. The aims of this study were to explore the in vivo relationship between passive fascicle length and passive sarcomere length at different muscle-tendon unit lengths and determine whether sarcomere and fascicle length relationships are the same in different regions of muscle. A microendoscopy needle probe capable of in vivo sarcomere imaging was inserted into a proximal location of the human tibialis anterior muscle at three different ankle positions [5° dorsiflexion, 5° plantar flexion (PF), and 15° PF] and one distal location at a constant ankle position (5° PF distal). Ultrasound imaging of tibialis anterior fascicles, centered on the location of the needle probe, was performed for each condition to estimate fascicle length. Sarcomere length and fascicle length increased with increasing muscle-tendon unit length, although the correlation between sarcomere length change and muscle fascicle length change was only moderate ( r2 = 0.45). Passive sarcomere length was longer at the distal imaging site than the proximal site ( P = 0.01). When sarcomere number was estimated from sarcomere length and fascicle length, there were fewer sarcomeres in the fibers of distal location than the proximal location ( P = 0.01). These data demonstrate that fascicle length changes are representative of sarcomere length changes, although significant variability in sarcomere length exists within a muscle and sarcomere number per fiber is region-dependent. NEW & NOTEWORTHY Sarcomere and fascicle lengths were measured in vivo from human muscle to examine the relationship between the different scales of organization. Changes in fascicle length were moderately related to sarcomere length changes; however, sarcomere length and number per fiber varied from proximal to distal regions of the muscle. Differences in average sarcomere operating lengths across the muscle suggest potentially different stresses or strains experienced within different regions of muscle.

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Nonisometric behavior of fascicles during isometric contractions of a human muscle

Journal of Applied Physiology ◽

10.1152/jappl.1998.85.4.1230 ◽

1998 ◽

Vol 85 (4) ◽

pp. 1230-1235 ◽

Cited By ~ 143

Author(s):

Masamitsu Ito ◽

Yasuo Kawakami ◽

Yoshiho Ichinose ◽

Senshi Fukashiro ◽

Tetsuo Fukunaga

Keyword(s):

Young’S Modulus ◽

Joint Angle ◽

Young's Modulus ◽

Pennation Angle ◽

Human Muscle ◽

Isometric Contractions ◽

Fascicle Length ◽

Tendon Stiffness ◽

Tendon Elongation

Fascicle length, pennation angle, and tendon elongation of the human tibialis anterior were measured in vivo by ultrasonography. Subjects ( n = 9) were requested to develop isometric dorsiflexion torque gradually up to maximal at the ankle joint angle of 20° plantarflexion from the anatomic position. Fascicle length shortened from 90 ± 7 to 76 ± 7 (SE) mm, pennation angle increased from 10 ± 1 to 12 ± 1°, and tendon elongation increased up to 15 ± 2 mm with graded force development up to maximum. The tendon stiffness increased with increasing tendon force from 10 N/mm at 0–20 N to 32 N/mm at 240–260 N. Young’s modulus increased from 157 MPa at 0–20 N to 530 MPa at 240–260 N. It can be concluded that, in isometric contractions of a human muscle, mechanical work, some of which is absorbed by the tendinous tissue, is generated by the shortening of muscle fibers and that ultrasonography can be used to determine the stiffness and Young’s modulus for human tendons.

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Changes in force and tendinous tissue elongation during the early phase of tetanic summation in in vivo human tibialis anterior muscle

Journal of Biomechanics ◽

10.1016/j.jbiomech.2009.11.015 ◽

2010 ◽

Vol 43 (5) ◽

pp. 998-1001 ◽

Cited By ~ 5

Author(s):

Yoichi Ohta ◽

Norihiro Shima ◽

Kyonosuke Yabe

Keyword(s):

Early Phase ◽

Tibialis Anterior ◽

Tibialis Anterior Muscle ◽

Human Tibialis Anterior Muscle

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M-wave potentiation after voluntary contractions of different durations and intensities in the tibialis anterior

Journal of Applied Physiology ◽

10.1152/japplphysiol.01144.2014 ◽

2015 ◽

Vol 118 (8) ◽

pp. 953-964 ◽

Cited By ~ 13

Author(s):

Javier Rodriguez-Falces ◽

Jacques Duchateau ◽

Yoshiho Muraoka ◽

Stéphane Baudry

Keyword(s):

Tibialis Anterior ◽

Compound Action Potential ◽

Pennation Angle ◽

Second Phase ◽

Median Frequency ◽

Fascicle Length ◽

M Wave ◽

Muscle Fascicle ◽

Phase Amplitude ◽

Voluntary Contractions

The study was undertaken to provide insight into the mechanisms underlying the potentiation of the muscle compound action potential (M wave) after conditioning contractions. M waves were evoked in the tibialis anterior before and after isometric maximal voluntary contractions (MVC) of 1, 3, 6, 10, 30, and 60 s, and after 3-s contractions at 10, 30, 50, 70, 90, and 100% MVC. The amplitude, duration, and area of the first and second phases of the M wave, together with the median frequency (Fmedian) and muscle fiber conduction velocity (MFCV) were recorded. Furthermore, twitch force, muscle fascicle length, and pennation angle were measured at rest, before, and 1 s after the conditioning contractions. The results indicate that only the amplitude of the second phase of the M wave was significantly increased after conditioning contractions. The extent of this potentiation was similar for MVC durations ranging from 1 to 10 s and augmented progressively with contraction intensity from 30 to 70% MVC. After these conditioning contractions, the duration and area of the two M-wave phases decreased ( P < 0.05), whereas MFCV and Fmedian increased ( P < 0.05). For all of these parameters, the greatest changes occurred 1 s after the conditioning contraction. Changes in MFCV after the contractions were correlated with those in M-wave second-phase amplitude ( r2 = 0.42; P < 0.05) and Fmedian ( r2 = 0.53; P < 0.05). In contrast, fascicle length and pennation angle did not change after the conditioning contractions. It is concluded that the potentiation of the second phase of the M wave is mainly due to an increased MFCV.

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Tendinous movement of a human muscle during voluntary contractions determined by real-time ultrasonography

Journal of Applied Physiology ◽

10.1152/jappl.1996.81.3.1430 ◽

1996 ◽

Vol 81 (3) ◽

pp. 1430-1433 ◽

Cited By ~ 66

Author(s):

T. Fukunaga ◽

M. Ito ◽

Y. Ichinose ◽

S. Kuno ◽

Y. Kawakami ◽

...

Keyword(s):

Real Time ◽

Ankle Joint ◽

Plantar Flexion ◽

Tibialis Anterior Muscle ◽

Human Muscle ◽

Muscle Physiology ◽

Angular Change ◽

Potential Applications ◽

Voluntary Contractions ◽

Real Time Ultrasonography

The degree of shortening or lengthening of muscles during joint actions has not been clarified in humans, although such information is essential in understanding human muscle functions. In this study, the tendinous movement of a muscle was determined by real-time ultrasonography during voluntary contractions. The tibialis anterior muscle (TA) was tested in five healthy men who performed dorsi- and plantar flexion movements (shortening and lengthening of TA) at two frequencies (0.1 and 1.5 Hz). The insertion point (eta) of fascicles onto the aponeurosis was clearly visualized on the ultrasonogram, and its position relative to a fixed marker moved proximally and distally according to dorsi- and plantar flexion of ankle joint. The movement of eta occurred in phase with the angular change of ankle joint, giving high correlations (r = 0.93 to 0.97) between the displacement of eta and the angle. The displacement of eta for one radian of joint angle change, 46.5 +/- 1.7 (SD) mm, was comparable to the reported moment arm of TA. The present method has many potential applications in the field of muscle physiology and biomechanics in humans.

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In vivo measurement of fascicle length and pennation of the human anconeus muscle at several elbow joint angles

Journal of Anatomy ◽

10.1111/joa.12233 ◽

2014 ◽

Vol 225 (5) ◽

pp. 502-509 ◽

Cited By ~ 3

Author(s):

Daniel E. Stevens ◽

Cameron B. Smith ◽

Brad Harwood ◽

Charles L. Rice

Keyword(s):

Elbow Joint ◽

Joint Angles ◽

Fascicle Length ◽

In Vivo Measurement

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Three-dimensional geometrical changes of the human tibialis anterior muscle and its central aponeurosis measured with three-dimensional ultrasound during isometric contractions

PeerJ ◽

10.7717/peerj.2260 ◽

2016 ◽

Vol 4 ◽

pp. e2260 ◽

Cited By ~ 36

Author(s):

Brent J. Raiteri ◽

Andrew G. Cresswell ◽

Glen A. Lichtwark

Keyword(s):

Three Dimensional ◽

Muscle Length ◽

Pennation Angle ◽

Human Muscle ◽

Muscle Fibres ◽

Isometric Contractions ◽

Fascicle Length ◽

Cross Sectional ◽

Shape Changes

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.

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