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Mechanical Properties of Aponeurosis and Tendon of the Cat Soleus Muscle During Whole-Muscle Isometric Contractions

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Mechanical Properties of Aponeurosis and Tendon of the Cat Soleus Muscle During Whole-Muscle Isometric Contractions JOURNAL OF MORPHOLOGY 224:73-86 (1995) Mechanical Properties of Aponeurosis and Tendon of the Cat Soleus Muscle During Whole-Muscle Isometric Contractions STEPHEN H. SCOTT AND GERALD E. LOEB MRC Group in Sensory-Motor Physiology, Department of Physiology, Queen's University, Kingston, Ontario, Canada K7L 3N6 ABSTRACT Recent studies have suggested that the mechanical properties of aponeurosis are not similar to the properties of external tendon. In the present study, the lengths of aponeurosis, tendon, and muscle fascicles were recorded individually, using piezoelectric crystals attached to the surface of each struc- ture during isometric contractions in the cat soleus muscle. We used a surgical microscope to observe the surface of the aponeurosis, which revealed a confound- ing effect on measures of aponeurosis length due to sliding of a thin layer of epimysium over the proximal aponeurosis. After correcting for this artifact, the stiffness computed €or aponeurosis was similar to tendon, with both increasing from around 8 Fo/L, (Fo is maximum isometric force and Lc is tissue length) at 0.1 Fo to 30 Fo/L, at forces greater than 0.4 Fo. At low force levels only (0.1 Fo), aponeurotic stiffness increased somewhat as fascicle length increased. There was a gradient in the thickness of the aponeurosis along its length: its thickness was minimal at the proximal end and maximal at the distal end, where it converged to form the external tendon. This gradient in thickness appeared to match the gradient in tension transmitted along this structure. We conclude that the specific mechanical properties of aponeurosis are similar to those of tendon. o 1995 Wiley-Liss, Inc. The contractile components of muscle ex- from muscles representing a wide range of ert forces on the relatively rigid skeleton via musculotendinous architectures. in-series connective tissue. The mechanical An alternative to the study of whole arrangements and properties of these connec- muscles is to develop models of particular tive tissues may have important effects on muscles based on general mechanical func- the dynamics and energetics of the relation- tions provided by the various individual tis- ship between muscle fascicles and skeleton. sues of which they are composed: contractile For example, spring-like compliance in the components, parallel-elastic components, se- connective tissue may absorb and release elas- ries-elastic components and the mechanical tic strain energy (Alexander and Vernon, '75; coupling among them. The mechanical func- Cavagna, '77) and may distort the relation- tions that reside wholly within the external ship between the overall length of a muscle tendon or individual muscle fibers are ame- and the proprioceptive feedback from length nable to study in isolated preparations of those tissues (e.g., Ker, '81 and Edman, '88, sensors such as muscle spindles (Rack and respectively). However, the muscle fibers of Westbury, '84; Hoffer et al., '89; Griffiths, many muscles are attached not to tendon or '91, but see Elek et al., '90). The magnitude bone, but rather to sheets of internal and/or of these effects usually depends on the spe- external connective tissue called aponeuro- cific morphometry of the muscle, and extrapo- ses. The mechanical properties of an exten- lation to other muscles requires an explicit or sive aponeurosis may dominate the series- implicit mathematical description. However, the selection of the qualitative form and par- ticular quantitative values for the compo- Address reprint requests to Dr. G.E. Loeb, Bio-MedicalEngineer- ingunit, Queen's University, Kingston, Ontario,K7L 3N6 Canada. nents of the model of whole muscle is ham- Dr. S.H. Scott is now at the Departement de Physiologie, pered by the paucity of experimental data Universite de Montreal, Montrdal, Qu&ec, H3C 357 Canada. o 1995 WILEY-LISS, INC. 74 S.H. SCOTT AND G.E. LOEB elastic and mechanical coupling functions, grammed sequences of electrical stimuli to but these properties are not well understood. the nerve entering soleus (50 Hz for 400 ms) The intimate and distributed connections while controlling the position and velocity of between an aponeurosis and terminating a step-motor attached in-series to the muscle. muscle fibers make it difficult to estimate its Whole muscle isometric contractions were mechanical properties directly. Techniques recorded at 16 lengths that evenly spanned such as photogrammetry have been em- the anatomical range of motion of soleus. ployed only recently to record length changes The program recorded the force generated by of connective tissue during changes in muscle the muscle and the position of the motor, force (Huijing and Ettema, '88/89; Ettema which was calibrated in terms of whole- and Huijing, '89; Lieber et al., '91; Zuurbier muscle length. The program also recorded et al. '94). Based on such data, Lieber et al. the length of individual portions of the muscle ('91) suggest that aponeurosis and tendon (fascicle, aponeurosis and tendon) using pi- have very different mechanical properties: ezoelectric crystaIs (Sonomicrometer 120; aponeurosis was found to be four times more Triton Technology) attached to the surface of compliant than tendon. Recently Ettema and the muscle. The crystals transmitted ultra- Huijing ('89) claimed to have shown that the sonic pulses through a pool of parrafin oil; length of an aponeurosis is dependent not the pool was created by tethering the skin only on muscle force, but also on fascicle flaps to a metal ring. Each ultrasonic pulse length. These studies suggest that the organi- was transmitted by one crystal and received zation of an aponeurosis is complex and that by another; the transit time was converted its mechanical properties are not similar to into a measure of length. The transmission external tendon. of ultrasonic pulses through the paraffin oil, In the present study multiple piezoelectric rather than directly through the muscle tis- crystals were attached to the surface of the sue (i.e., Griffiths, '91; Hoffer et al., '89) cat soleus muscle. These provided direct mea- negates the conflicting effect of muscle force surement of the length of the aponeurosis on the velocity of the ultrasonic signals (see and tendon during isometric contractions per- Hatta et al., '88; Caputi et al., '92). Some formed at different whole-muscle lengths. preliminary experiments were performed in These recordings were used to estimate the which the crystals were attached to a Silastic stiffness properties of the tendon and aponeu- sheet (Reinforced Silastic Sheeting, Dow rosis. In addition, anatomical techniques were Corning) that was sutured to the muscle used to relate the structure of the aponeuro- sis to its mechanical properties. surface. In subsequent experiments, the crys- tals were attached to the surface of the muscle MATERIALS AND METHODS using cyanoacrylate adhesive (Accu-Flo Crazy Data collection Glue, Lepage). Crystals attached by the adhe- Experiments were carried out on adult cats sive were found to remain secure for long (2.75-4.7 kg; either sex) anesthetized ini- periods of time, although constant monitor- tially with 35 mg/kg of sodium pentobarbital ing was required in order to ensure the stabil- IP with supplemental doses IV as needed to ity and alignment of the crystals and thus the suppress withdrawal reflex. An incision was quality of the output signals. Although the made along the posterior surface of the right glue may tend to augment the stiffness prop- leg from the calcaneum to the popliteal fossa. erties of the aponeurosis, the magnitude The popliteal fat pad was removed and the would be minimal since the size of the drop of plantaris and gastrocnemius muscles were glue was small relative to the distance tra- resected. A tri- or bipolar nerve cuff was versed between crystals (approx. 1:15). placed around the tibial nerve. Nerve stimu- Crystals were positioned initially at the lation was elicited by a biphasic constant proximal and distal ends of the aponeurosis current pulse with a duration of 0.2 ms and to record the entire length of this structure. an amplitude of four times the current to The distal end of the aponeurosis was defined elicit a just-visible contraction. The soleus as the most distal point of muscle-fiber attach- tendon and a small piece of the posterior ment. Most of the aponeurosis appears as calcaneus were removed from the foot and longitudinal white strands of connective tis- attached to a force transducer (linear up to sue that converge to form the external ten- 55 N), which was attached to a stepping don. However, the proximal end of the apo- motor. A computer-controlled data-acquisi- neurosis is less evident; its border can best be tion system was used to deliver prepro- visualized at long muscle lengths when the MECHANICAL PROPERTIES OF AF’ONEUROSIS AND TENDON 75 perimeter of the aponeu:. -sis can be seen as a 0.1 Fo above and below the desired force level change in light reflectance due to the angular (Fig. 1).Stiffness estimates were normalized change between the surfxe of the fascicles to Fo for each preparation and to L,, the and aponeurosis. length of the recorded tissue at slack length The length of the entire aponeurosis was and zero muscle force, in order to define a recorded by one set of crystals in the first few dimensionless term called the “specific stiff- experiments. In later experiments, a crystal ness” of the tissue. To determine the stiff- was positioned in the middle of the aponeuro- ness of a particular muscle’s connective tis- sis, and the lengths of the distal and proximal sue, the dimensionlessspecific stiffness would portions of the aponeurosis were recorded be multiplied by that muscle’s Fo (typically simultaneous, In the last three experi- estimated from its physiological cross-sec- ments, crystals ./ re also attached on the tional area in cm2 and the specific tension of medial and lateral edqes of the aponeurosis muscle in N/cm2) and divided by its L, (in so that the width of this structure could be cm) resulting in N/cm.
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