Adaptations in human neuromuscular function following prolonged unweighting: I. Skeletal muscle contractile properties and applied ischemia efficacy

Strength loss following disuse may result from alterations in muscle and/or neurological properties. In this paper, we report our findings on human plantar flexor muscle properties following 4 wk of limb suspension (unilateral lower limb suspension), along with the effect of applied ischemia (Isc) on these properties. In the companion paper (Part II), we report our findings on the changes in neurological properties. Measurements of voluntary and evoked forces, the compound muscle fiber action potential (CMAP), and muscle cross-sectional area (CSA) were collected before and after 4 wk of unilateral lower limb suspension in adults ( n = 18; 19–28 yr). A subset of subjects ( n = 6) received applications of Isc 3 days/wk (3 sets; 5-min duration). In the subjects not receiving Isc, the loss in CSA and strength was as expected (∼9 and 14%). We observed a 30% slowing in the duration of the CMAP, a 10% decrease in evoked doublet force, a 12% increase in the twitch-to-doublet force ratio, and an altered postactivation potentiation response (11% increase in the postactivation potentiation-to-doublet ratio). We also detected a 10% slowing in the ability of the plantar flexor to develop force during the initial phase of an evoked contraction, along with a 6% reduction in in vivo specific doublet force. In the Isc subjects, no preservation was observed in strength or the evoked muscle properties. However, the Isc group did maintain CSA of the lateral gastrocnemius, as the control subjects’ lateral gastrocnemius atrophied 10.2%, whereas the subjects receiving Isc atrophied 4.7%. Additionally, Isc abolished the unweighting-induced slowing in the CMAP. These findings suggest that unweighting alters the contractile properties involved in the excitation-contraction coupling processes and that Isc impacts the sarcolemma.

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Differences in Plantar Flexor Fascicle Length and Pennation Angle between Healthy and Poststroke Individuals and Implications for Poststroke Plantar Flexor Force Contributions

Stroke Research and Treatment ◽

10.1155/2014/919486 ◽

2014 ◽

Vol 2014 ◽

pp. 1-6 ◽

Cited By ~ 4

Author(s):

John W. Ramsay ◽

Thomas S. Buchanan ◽

Jill S. Higginson

Keyword(s):

Pennation Angle ◽

Medial Gastrocnemius ◽

Plantar Flexor ◽

Flexor Muscle ◽

Fascicle Length ◽

Cross Sectional ◽

Lateral Gastrocnemius ◽

Relative Contribution ◽

Muscle Fascicle ◽

The Individual

Poststroke plantar flexor muscle weakness has been attributed to muscle atrophy and impaired activation, which cannot collectively explain the limitations in force-generating capability of the entire muscle group. It is of interest whether changes in poststroke plantar flexor muscle fascicle length and pennation angle influence the individual force-generating capability and whether plantar flexor weakness is due to uniform changes in individual muscle force contributions. Fascicle lengths and pennation angles for the soleus, medial, and lateral gastrocnemius were measured using ultrasound and compared between ten hemiparetic poststroke subjects and ten healthy controls. Physiological cross-sectional areas and force contributions to poststroke plantar flexor torque were estimated for each muscle. No statistical differences were observed for any muscle fascicle lengths or for the lateral gastrocnemius and soleus pennation angles between paretic, nonparetic, and healthy limbs. There was a significant decrease (P<0.05) in the paretic medial gastrocnemius pennation angle compared to both nonparetic and healthy limbs. Physiological cross-sectional areas and force contributions were smaller on the paretic side. Additionally, bilateral muscle contributions to plantar flexor torque remained the same. While the architecture of each individual plantar flexor muscle is affected differently after stroke, the relative contribution of each muscle remains the same.

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In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men

Journal of Applied Physiology ◽

10.1152/japplphysiol.01186.2004 ◽

2005 ◽

Vol 99 (3) ◽

pp. 1050-1055 ◽

Cited By ~ 138

Author(s):

Christopher I. Morse ◽

Jeanette M. Thom ◽

Neil D. Reeves ◽

Karen M. Birch ◽

Marco V. Narici

Keyword(s):

Achilles Tendon ◽

Voluntary Contraction ◽

Pennation Angle ◽

Specific Force ◽

Plantar Flexor ◽

Moment Arm ◽

Plantar Flexors ◽

Elderly Men ◽

Cross Sectional

Sarcopenia and muscle weakness are well-known consequences of aging. The aim of the present study was to ascertain whether a decrease in fascicle force (Ff) could be accounted for entirely by muscle atrophy. In vivo physiological cross-sectional area (PCSA) and specific force (Ff/PCSA) of the lateral head of the gastrocnemius (GL) muscle were assessed in a group of elderly men [EM, aged 73.8 yr (SD 3.5), height 173.4 cm (SD 4.4), weight 78.4 kg (SD 8.3); means (SD)] and for comparison in a group of young men [YM, aged 25.3 yr (SD 4.4), height 176.4 cm (SD 7.7), weight 79.1 kg (SD 11.9)]. GL muscle volume (Vol) and Achilles tendon moment arm length were evaluated using magnetic resonance imaging. Pennation angle and fiber fascicle length (Lf) were measured using B-mode ultrasonography during isometric maximum voluntary contraction of the plantar flexors. PCSA was estimated as Vol/Lf. GL Ff was calculated by dividing Achilles tendon force by the cosine of θ, during the interpolation of a supramaximal doublet, and accounting for antagonist activation level (assessed using EMG), Achilles tendon moment arm length, and the relative PCSA of the GL within the plantar flexor group. Voluntary activation of the plantar flexors was lower in the EM than in the YM (86 vs. 98%, respectively, P < 0.05). Compared with the YM, plantar flexor maximal voluntary contraction torque and Ff of the EM were lower by 47 and 40%, respectively ( P < 0.01). Both Vol and PCSA were smaller in the EM by 28% ( P < 0.01) and 16% ( P < 0.05), respectively. Also, pennation angle was 12% smaller in the EM, whereas there was no significant difference in Lf between the YM and EM. After accounting for differences in agonists and antagonists activation, the Ff/PCSA of the EM was 30% lower than that of the YM ( P < 0.01). These findings demonstrate that the loss of muscle strength with aging may be explained not only by a reduction in voluntary drive to the muscle, but mostly by a decrease in intrinsic muscle force. This phenomenon may possibly be due to a reduction in single-fiber specific tension.

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Subperiosteal expansion and cortical remodeling of the human femur and tibia with aging

Science ◽

10.1126/science.7112107 ◽

1982 ◽

Vol 217 (4563) ◽

pp. 945-948 ◽

Cited By ~ 221

Author(s):

CB Ruff ◽

WC Hayes

Keyword(s):

Cross Sections ◽

Lower Limb ◽

Torsional Rigidity ◽

American Southwest ◽

Cross Sectional ◽

Human Femur ◽

Second Moments

Increases with aging in subperiosteal dimensions and second moments of area (measures of bending and torsional rigidity) in femoral and tibial cross sections are documented in an archeological sample from the American Southwest. Significant differences between cross-sectional sites and between sexes in the pattern of cortical remodeling with age are also present. These differences appear to be related to variations in the stress or strain levels in different regions of the femur and tibia which result from in vivo mechanical loadings of the lower limb.

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Series elasticity facilitates safe plantar flexor muscle–tendon shock absorption during perturbed human hopping

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2021.0201 ◽

2021 ◽

Vol 288 (1947) ◽

Author(s):

Taylor J. M. Dick ◽

Christofer J. Clemente ◽

Laksh K. Punith ◽

Gregory S. Sawicki

Keyword(s):

Steady State ◽

Neuromuscular Control ◽

Ground Contact ◽

Plantar Flexor ◽

Plantar Flexors ◽

Flexor Muscle ◽

Unpredictable Environments ◽

Co Activation ◽

Length Changes

In our everyday lives, we negotiate complex and unpredictable environments. Yet, much of our knowledge regarding locomotion has come from studies conducted under steady-state conditions. We have previously shown that humans rely on the ankle joint to absorb energy and recover from perturbations; however, the muscle–tendon unit (MTU) behaviour and motor control strategies that accompany these joint-level responses are not yet understood. In this study, we determined how neuromuscular control and plantar flexor MTU dynamics are modulated to maintain stability during unexpected vertical perturbations. Participants performed steady-state hopping and, at an unknown time, we elicited an unexpected perturbation via rapid removal of a platform. In addition to kinematics and kinetics, we measured gastrocnemius and soleus muscle activations using electromyography and in vivo fascicle dynamics using B-mode ultrasound. Here, we show that an unexpected drop in ground height introduces an automatic phase shift in the timing of plantar flexor muscle activity relative to MTU length changes. This altered timing initiates a cascade of responses including increased MTU and fascicle length changes and increased muscle forces which, when taken together, enables the plantar flexors to effectively dissipate energy. Our results also show another mechanism, whereby increased co-activation of the plantar- and dorsiflexors enables shortening of the plantar flexor fascicles prior to ground contact. This co-activation improves the capacity of the plantar flexors to rapidly absorb energy upon ground contact, and may also aid in the avoidance of potentially damaging muscle strains. Our study provides novel insight into how humans alter their neural control to modulate in vivo muscle–tendon interaction dynamics in response to unexpected perturbations. These data provide essential insight to help guide design of lower-limb assistive devices that can perform within varied and unpredictable environments.

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Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. I. Influence of motoneurons on muscle

Journal of Neurophysiology ◽

10.1152/jn.1987.57.4.1210 ◽

1987 ◽

Vol 57 (4) ◽

pp. 1210-1226 ◽

Cited By ~ 25

Author(s):

R. C. Foehring ◽

G. W. Sypert ◽

J. B. Munson

Keyword(s):

Motor Unit ◽

Muscle Fibers ◽

Motor Units ◽

Contractile Properties ◽

Medial Gastrocnemius ◽

Similar Degree ◽

Muscle Properties ◽

Lateral Gastrocnemius ◽

Type Distribution ◽

Unit Type

This study addresses two questions: is reinnervation of mammalian skeletal muscle selective with respect to motor-unit type? And to what degree may muscle-unit contractile properties be determined by the motoneuron? Properties of individual motor units were examined following cross-reinnervation (X-reinnervation) of lateral gastrocnemius (LG) and soleus muscles by the medial gastrocnemius (MG) nerve in the cat. We examined animals at two postoperative times: 9-10 wk (medX) and 9-11 mo (longX). For comparison, properties of normal LG and soleus motor units were studied. Motor units were classified on the basis of their contractile response as fast contracting fatigable, fast intermediate, fast contracting fatigue resistant, or slow (types FF, FI, FR, or S, respectively) (13,29). Muscle fibers were classified on the basis of histochemical properties as fast glycolytic, fast oxidative glycolytic, or slow oxidative (types FG, FOG, or SO, respectively) (61). Reinnervation of LG and soleus was not selective with respect to motor-unit type. Both muscles were innervated by a full complement of MG motoneuron types, apparently in normal MG proportions. MG motoneurons determined LG muscle fibers' properties to a similar degree as reinnervated MG muscle fibers. In contrast, soleus muscle fibers "resisted" the influence of MG motoneurons. Thus, although longX-reinnervated LG muscle (longX LG) had a motor-unit type distribution similar to normal or self-reinnervated MG, longX soleus contained predominantly type S motor units. Overall mean values for muscle-unit contractile properties reflected this motor-unit type distribution. Muscle units in longX LG and longX soleus had contractile properties typical of the same motor-unit type in normal LG or soleus, respectively. Motor-unit types were recognizable at 10 wk X-reinnervation, although muscle-unit tensions were lower than after 10 mo. The proportions of fast and slow motor units in medX LG were similar to longX LG, although a greater proportion of fast units were resistant to fatigue at 10 wk. There were fewer fast units in medX soleus than longX soleus, which suggested that motor-unit type conversion or innervation of muscle fibers by fast motoneurons is not complete at 10 wk. We conclude that reinnervation of the LG and soleus muscles by MG motoneurons was not selective with respect to motor-unit type. MG motoneurons determined LG muscle properties to a similar degree as self-reinnervated MG muscle fibers. Soleus muscle fibers resisted the influence of MG motoneurons, representing a limit to neural determination of muscle properties.

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Comparison Between Foam Rolling With and Without Vibration on Passive and Active Plantar Flexor Muscle Properties

The Journal of Strength and Conditioning Research ◽

10.1519/jsc.0000000000004123 ◽

2021 ◽

Vol Publish Ahead of Print ◽

Author(s):

Masatoshi Nakamura ◽

Shigeru Sato ◽

Ryosuke Kiyono ◽

Riku Yoshida ◽

Koki Yasaka ◽

...

Keyword(s):

Plantar Flexor ◽

Flexor Muscle ◽

Muscle Properties ◽

Foam Rolling

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Triceps surae torque-length relationships relevant for walking activity levels with and without an ankle exoskeleton

10.1101/778175 ◽

2019 ◽

Author(s):

Anthony L. Hessel ◽

Brent J. Raiteri ◽

Michael J. Marsh ◽

Daniel Hahn

Keyword(s):

Muscle Activity ◽

Metabolic Cost ◽

Activity Levels ◽

Plantar Flexor ◽

Plantar Flexors ◽

Flexor Muscle ◽

Fascicle Length ◽

Lateral Gastrocnemius ◽

Work Requirements ◽

Ankle Exoskeleton

AbstractAnkle exoskeletons have been developed to assist walking by offloading the plantar flexors work requirements, which reduces muscle activity level. However, reduced muscle activity alters plantar flexor muscle-tendon unit dynamics in a way that is poorly understood. We therefore evaluated torque-fascicle length properties of the soleus and lateral gastrocnemius during voluntary contractions at simulated activity levels typical during late stance with and without an ankle exoskeleton. Soleus activity levels (100, 30, and 22% maximal voluntary activity) were produced by participants via visual electromyography feedback at ankle angles ranging from −10° plantar flexion to 35° dorsiflexion. Using dynamometry and ultrasound imaging, torque-fascicle length data of the soleus and lateral gastrocnemius were produced. The results indicate that muscle activity reductions observed with an exoskeleton shift the torque-angle and torque-fascicle length curves to more dorsiflexed ankle angles and longer fascicle lengths where no descending limb is physiologically possible. This shift is in line with previous simulations that predicted a similar increase in the operating fascicle range when wearing an exoskeleton. These data suggest that a small reduction in muscle activity causes changes to torque-fascicle length properties, which has implications for the design and testing of future ankle exoskeletons for assisted walking.Significance StatementAssistive lower-limb exoskeletons reduce the metabolic cost of walking by reducing the positive work requirements of the plantar flexor muscles. However, if the exoskeleton reduces plantar flexor muscle activity too much, then the metabolic benefit is lost. The biological reasons for this are unclear and hinder further exoskeleton development. This research study is the first to directly evaluate if a reduction in plantar flexor muscle activity similar to that caused by wearing an exoskeleton affects muscle function. We found that reduced muscle activity changes the torque-length properties of two plantar flexors, which could explain why reducing muscle activity too much can increase metabolic cost.

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Recovery of muscle transfers replacing the total plantar flexor muscle group in rats

Journal of Applied Physiology ◽

10.1152/jappl.1998.84.6.1865 ◽

1998 ◽

Vol 84 (6) ◽

pp. 1865-1871 ◽

Cited By ~ 4

Author(s):

Stephanie W. Miller ◽

Cheryl A. Hassett ◽

John A. Faulkner

Keyword(s):

Isometric Force ◽

Force Production ◽

Plantar Flexor ◽

Flexor Muscle ◽

Average Force ◽

Cross Sectional ◽

Individual Control ◽

Control Value ◽

Muscle Transfers ◽

Synergistic Muscles

In rats, combinations of plantar flexor muscles representing ∼20, 40, 60, and 80% of the mass of the total plantar flexor group were transferred orthotopically in the absence of synergistic muscles and allowed to recover for 120 days. We hypothesized that, compared with their individual control values for structural and functional variables, the transfers would display a hierarchical array of deficits, proportional to their initial mass and, consequently, inversely proportional to the relative load on the transfers. Surprisingly, compared with their individual control values, each muscle transfer displayed deficits of 30–40% in muscle mass, total fiber cross-sectional area, and maximum isometric force, with the exception of the smallest transfer, the plantaris (PLN) muscle, which recovered 100% of its control value for each of these variables. Therefore, except for the PLN transfer, the muscle transfers studied displayed deficits similar in magnitude to those reported for muscles transferred in the presence of synergistic muscles. The greater recovery of the PLN transfer was attributed to the relatively large requirement for force production imposed on this transfer due to the average force requirements of the total plantar flexor group.

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Comparison of Twitch-Contractile Properties of Plantar-Flexor Muscles in Young and 52- to 63-Year-Old Men

Journal of Aging and Physical Activity ◽

10.1123/japa.10.2.160 ◽

2002 ◽

Vol 10 (2) ◽

pp. 160-168 ◽

Cited By ~ 3

Author(s):

Mati Pääsuke ◽

Jaan Ereline ◽

Helena Gapeyeva ◽

Heigo Maamägi

Keyword(s):

Middle Age ◽

Voluntary Contraction ◽

Contractile Properties ◽

Plantar Flexor ◽

Postactivation Potentiation ◽

Force Development ◽

Flexor Muscles ◽

Contraction Times ◽

Old Men ◽

Plantar Flexor Muscles

This study compared maximal voluntary-contraction (MVC) force and twitch-contractile properties of the plantar-flexor muscles in resting and postactivation potentiation slates of 2 groups of men matched for similar levels of physical activity: young (19- to 22-year-olds. n = 13) and 52–63 years old (n = 12). MVC force, twitch peak force (PT), maximal rates of force development and relaxation, and postactivation potentiation were higher (p < .05) in young than in 52- to 63-year-old men. In young men. potentiated-twitch PT was 23.3% higher (p < .01) than resting twitch. Resting- and potentialed-twitch-contraction times were 16.7% and 18.3% shorter, respectively (p < .001), in young than in 52- to 63-year-old men. These Findings suggest that late middle age is characterized by reduced capacity for evoked twitch-force generation and potentiation and slowed speed of contraction of the plantar-flexor muscles.

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