Huub Maas

Intermuscular interaction via myofascial force transmission: effects of tibialis anterior and extensor hallucis longus length on force transmission from rat extensor digitorum longus muscle

Force transmission in rat anterior crural compartment, containing tibialis anterior (TA), extensor hallucis longus (EHL) and extensor digitorum longus (EDL) muscles, was investigated. These muscles together with the muscles of the peroneal compartment were excited maximally. Force was measured at both proximal and distal tendons of EDL muscle as well as at the tied distal tendons of TA and EHL muscles (the TA + EHL complex). Effects of TA + EHL complex length and force on proximally and distally measured forces of EDL muscle kept at constant muscle-tendon complex length were assessed. Length changes of EDL muscle were imposed by movement of the proximal force transducer to different positions.Proximal EDL force was unequal to distal EDL force (active as well as passive) over a wide range of EDL muscle-tendon complex lengths. This is an indication that force is also transmitted out of EDL muscle via pathways other than the tendons (i.e. inter- and/or extramuscular myofascial force transmission). At constant low EDL length, distal lengthening of the TA + EHL complex increased proximal EDL force and decreased distal EDL force. At optimum EDL length, TA+EHL active force was linearly related to the difference between proximal and distal EDL active force. These results indicate intermuscular myofascial force transmission between EDL muscle and the TA + EHL complex. The most likely pathway for this transmission is via connections of the intact intermuscular connective tissue network. The length effects of the TA + EHL complex can be understood on the basis of changes in the configuration, and consequently the stiffness, of these connections. Damage to connective tissue of the compartment decreased the proximo-distal EDL force difference, which indicates the importance of an intact connective tissue network for force transmission from muscle fibers to bone.

Implantable Myoelectric Sensors (IMESs) for Intramuscular Electromyogram Recording

We have developed a multichannel electrogmyography sensor system capable of receiving and processing signals from up to 32 implanted myoelectric sensors (IMES). The appeal of implanted sensors for myoelectric control is that electromyography (EMG) signals can be measured at their source providing relatively cross-talk-free signals that can be treated as independent control sites. An external telemetry controller receives telemetry sent over a transcutaneous magnetic link by the implanted electrodes. The same link provides power and commands to the implanted electrodes. Wireless telemetry of EMG signals from sensors implanted in the residual musculature eliminates the problems associated with percutaneous wires, such as infection, breakage, and marsupialization. Each implantable sensor consists of a custom-designed application-specified integrated circuit that is packaged into a biocompatible RF BION capsule from the Alfred E. Mann Foundation. Implants are designed for permanent long-term implantation with no servicing requirements. We have a fully operational system. The system has been tested in animals. Implants have been chronically implanted in the legs of three cats and are still completely operational four months after implantation.

Force transmission between synergistic skeletal muscles through connective tissue linkages.

The classic view of skeletal muscle is that force is generated within its muscle fibers and then directly transmitted in-series, usually via tendon, onto the skeleton. In contrast, recent results suggest that muscles are mechanically connected to surrounding structures and cannot be considered as independent actuators. This article will review experiments on mechanical interactions between muscles mediated by such epimuscular myofascial force transmission in physiological and pathological muscle conditions. In a reduced preparation, involving supraphysiological muscle conditions, it is shown that connective tissues surrounding muscles are capable of transmitting substantial force. In more physiologically relevant conditions of intact muscles, however, it appears that the role of this myofascial pathway is small. In addition, it is hypothesized that connective tissues can serve as a safety net for traumatic events in muscle or tendon. Future studies are needed to investigate the importance of intermuscular force transmission during movement in health and disease.

Are skeletal muscles independent actuators? Force transmission from soleus muscle in the cat

It is unclear if skeletal muscles act mechanically as independent actuators. The purpose of the present study was to investigate force transmission from soleus (SO) muscle for physiological lengths as well as relative positions in the intact cat hindlimb. We hypothesized that force transmission from SO fibers will be affected by length changes of its two-joint synergists. Ankle plantar flexor moment on excitation of the SO was measured for various knee angles (70-140 degrees ). This involved substantial length changes of gastrocnemius and plantaris muscles. Ankle angle was kept constant (80 degrees -90 degrees ). However, SO ankle moment was not significantly affected by changes in knee angle; neither were half-relaxation time and the maximal rate of relaxation (P > 0.05). Following tenotomy, SO ankle moment decreased substantially (55 +/- 16%) but did not reach zero, indicating force transmission via connective tissues to the Achilles tendon (i.e., epimuscular myofascial force transmission). During contraction SO muscle shortened to a much greater extent than in the intact case (16.0 +/- 0.6 vs. 1.0 +/- 0.1 mm), which resulted in a major position shift relative to its synergists. If the SO was moved back to its position corresponding to the intact condition, SO ankle moment approached zero, and most muscle force was exerted at the distal SO tendon. Our results also suggested that in vivo the lumped intact tissues linking SO to its synergists are slack or are operating on the toe region of the stress-strain curve. Thus, within the experimental conditions of the present study, the intact cat soleus muscle appears to act mechanically as an independent actuator.

Muscle force is determined also by muscle relative position: isolated effects.

Effects on force of changes of the position of extensor digitorum longus muscle (EDL) relative to surrounding tissues were investigated in rat. Connective tissue at the muscle bellies of tibialis anterior (TA), extensor hallucis longus (EHL) and EDL was left intact, to allow myofascial force transmission. The position of EDL muscle was altered, without changing EDL muscle-tendon complex length, and force exerted at proximal and distal tendons of EDL as well as summed force exerted at the distal tendons of TA and EHL muscles (TA+EHL) were measured. Proximal and distal EDL forces as well as distal TA+EHL force changed significantly on repositioning EDL muscle. These muscle position-force characteristics were assessed at two EDL lengths and two TA+EHL lengths. It was shown that changes of muscle force with length changes of a muscle is the result of the length changes per se, as well as of changes of relative position of parts of the muscle. It is concluded that in addition to length, muscle position relative to its surroundings co-determines isometric muscle force.

Intermuscular interaction between synergists in rat originates from both intermuscular and extramuscular myofascial force transmission.

The purpose of the present study is to investigate the origin of mechanical interactions between the rat extensor digitorum longus (EDL) muscle and the grouped tibialis anterior and extensor hallucis longus muscles (TA+EHL). The proximal and distal tendons of EDL as well as the tied distal tendons of TA+EHL were transected and connected to force transducers. Connective tissues at the muscle bellies of the anterior crural compartment were left intact. Supramaximal stimulation of the common peroneal nerve activated all muscles maximally and simultaneously. Length-isometric force characteristics of distal TA+EHL were assessed. Simultaneously, forces exerted at the proximal and distal tendons of EDL, kept at constant muscle-tendon complex length and position, were measured. Intermuscular interaction was tested in two conditions: (a) after full longitudinal compartmental fasciotomy, and (b) after blunt dissection of the intermuscular connective tissue linkages between EDL and TA+EHL. Note that in the latter condition, intermuscular myofascial pathways were eliminated. In the initial condition, lengthening TA+EHL by 12 mm increased proximal (by 0.14 N, i.e. 9.5%) and decreased distal EDL force (by 0.21 N, i.e. 11.8%), despite the fact that EDL muscle-tendon complex length was kept constant. Blunt dissection decreased TA+EHL and distal EDL forces at low TA+EHL lengths only, while proximal EDL force decreased for all TA+EHL lengths tested. The dissection caused no changes in the TA+EHL length effects on proximal EDL force. In contrast, the amplitude of change in the distal EDL force curve decreased significantly (by 39%) subsequent to blunt dissection. It is concluded that mechanical interaction between synergists originates from both intermuscular as well as extramuscular connective tissues. The highest contribution, however, should be ascribed to the extramuscular pathway.

The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finite-element modeling.

BACKGROUND Effects of extramuscular connective tissues on muscle force (experimentally measured) and lengths of sarcomeres (modeled) were investigated in rat. It was hypothesized that changes of muscle-relative position affect the distribution of lengths of sarcomeres within muscle fibers. METHOD OF APPROACH The position of extensor digitorum longus muscle (EDL) relative to intact extramuscular connective tissues of the anterior crural compartment was manipulated without changing its muscle-tendon complex length. RESULTS Significant effects of EDL muscle relative position on proximal and distal EDL forces were found, indicating changes of extramuscular myofascial force transmission. EDL isometric force exerted at its proximal and distal tendons differed significantly. Finite-element modeling showed that the distribution of lengths of sarcomeres is altered by changes of muscle-relative position. CONCLUSIONS It is concluded that forces exerted on a muscle via extramuscular myofascial pathways augment distributions of lengths of sarcomeres within that muscle.

IMPLICATIONS OF MUSCLE RELATIVE POSITION AS A CO-DETERMINANT OF ISOMETRIC MUSCLE FORCE: A REVIEW AND SOME EXPERIMENTAL RESULTS

Force is transmitted from muscle fiber to bone via several pathways: (1) via the tendons (i.e. myotendinous force transmission), (2) via intermuscular connective tissue to adjacent muscles (i.e. intermuscular myofascial force transmission), (3) via structures other than muscles (i.e. extramuscular myofascial force transmission). In vivo, the position of a muscle relative to adjacent muscles changes due to differences in moment arm between synergists as well as due to the fact that some muscles span only one joint and other muscles more than one joint. The position of a muscle relative to non-muscular structures within a compartment is altered with each change of the length of the muscle. The aim of this article is to describe recent experimental results, as well as some new experimental data, that have elucidated the role of muscle relative position on force transmission from muscle. Furthermore, relevant literature is discussed, taking into consideration these new insights of muscle functioning. It is concluded that the position of a muscle relative to surrounding tissues is a major co-determinant of isometric muscle force. For muscles operating within their in vivo context of connective tissue, such position effects should be taken into account.

Modeling short-range stiffness of feline lower hindlimb muscles

The short-range stiffness (SRS) of skeletal muscles is a critical property for understanding muscle contributions to limb stability, since it represents a muscles capacity to resist external perturbations before reflexes or voluntary actions can intervene. A number of studies have demonstrated that a simple model, consisting of a force-dependent active stiffness connected in series with a constant passive stiffness, is sufficient to characterize the SRS of individual muscles over the entire range of obtainable forces. The purpose of this study was to determine if such a model could be used to characterize the SRS-force relationship in a number of architecturally distinct muscles. Specifically, we hypothesized that the active and passive stiffness components for a specific muscle can be estimated from anatomical measurements, assuming uniform active and passive stiffness properties across all muscles. This hypothesis was evaluated in six feline lower hindlimb muscle types with different motor unit compositions and architectures. The SRS-force relationships for each muscle type were predicted based on anatomical measurements and compared to experimental data. The model predictions were accurate to within 30%, when uniform scaling properties were assumed across all muscles. Errors were the greatest for the extensor digitorum longus (EDL). When this muscle was removed from the analysis, prediction errors dropped to less than 8%. Subsequent analyses suggested that these errors might have resulted from differences in the tendon elastic modulus, as compared to the other muscles tested.

Short-Term Motor Compensations to Denervation of Feline Soleus and Lateral Gastrocnemius Result in Preservation of Ankle Mechanical Output during Locomotion

Denervation of selected ankle extensors in animals results in locomotor changes. These changes have been suggested to permit preservation of global kinematic characteristics of the hindlimb during stance. The peak ankle joint moment is also preserved immediately after denervation of several ankle extensors in the cat, suggesting that the animal’s response to peripheral nerve injury may also be aimed at preserving ankle mechanical output. We tested this hypothesis by comparing joint moments and power patterns during walking before and after denervation of soleus and lateral gastrocnemius muscles. Hindlimb kinematics, ground reaction forces and electromyographic activity of selected muscles were recorded during level, downslope (–50%) and upslope (50%) walking before and 1–3 weeks after nerve denervation. Denervation resulted in increased activity of the intact medial gastrocnemius and plantaris muscles, greater ankle dorsiflexion, smaller knee flexion, and the preservation of the peak ankle moment during stance. Surprisingly, ankle positive power generated in the propulsion phase of stance was increased (up to 50%) after denervation in all walking conditions (p < 0.05). The obtained results suggest that the short-term motor compensation to denervation of lateral gastrocnemius and soleus muscles may allow for preservation of mechanical output at the ankle. The additional mechanical energy generated at the ankle during propulsion can result, in part, from increased activity of intact synergists, the use of passive tissues around the ankle and by the tendon action of ankle two-joint muscles and crural fascia.