Ryan J. Monti

Transmission of forces within mammalian skeletal muscles

Most models of in vivo musculoskeletal function fail to take into account the diversity of force trajectories defined by muscle fiber architecture. It has been shown for many muscles, across species, that muscle fibers commonly end within muscle fascicles without reaching a myotendinous junction, and that many of these fibers show a progressive decline in cross-sectional area along the length of the muscle. The significance of these anatomical observations is that the tapering would seem to preclude forces generated at the largest cross-sectional area of the fibers being transmitted to the sarcomeres toward the ends of the tapered fiber. If all of the forces are transmitted via the sarcomeres arranged in series, those few sarcomeres at the smaller ends of the fibers must tolerate the stress exerted by the more numerous sarcomeres arranged in parallel at the portions of the fiber with larger cross-sectional areas. A logical alternative would be for forces to be transmitted laterally along the length of a fiber to the cell membrane and the extracellular matrix. Such a structural arrangement would permit an alternative force transmission vector and minimize the necessity for a precise level of force to be generated along the entire length of a fiber. There are cytoarchitectural and biochemical data demonstrating the presence of a subcellular network which is appropriately located to transmit forces from the active intracellular contractile elements to the extracellular intramuscular connective tissues. However, to fully comprehend how forces are transmitted from individual cross bridges to the tendon, it will be necessary to understand the interactions of all of the components of the muscle tendon complex from the molecular to the multicellular level. It is insufficient to know the physiology of the individual components in a restricted experimental paradigm and assume that these conditions account for the functional characteristics in vivo. Thus, the challenge is to understand how the sarcomeres and all of the associated structures transmit the forces of the whole muscle to its attachments.

Role of motor unit structure in defining function

Motor units, defined as a motoneuron and all of its associated muscle fibers, are the basic functional units of skeletal muscle. Their activity represents the final output of the central nervous system, and their role in motor control has been widely studied. However, there has been relatively little work focused on the mechanical significance of recruiting variable numbers of motor units during different motor tasks. This review focuses on factors ranging from molecular to macroanatomical components that influence the mechanical output of a motor unit in the context of the whole muscle. These factors range from the mechanical properties of different muscle fiber types to the unique morphology of the muscle fibers constituting a motor unit of a given type and to the arrangement of those motor unit fibers in three dimensions within the muscle. We suggest that as a result of the integration of multiple levels of structural and physiological levels of organization, unique mechanical properties of motor units are likely to emerge.

Mechanical properties of rat soleus aponeurosis and tendon during variable recruitment in situ.

SUMMARY The in vitro mechanical properties of tendons are well described, whereas little data exist for conditions mimicking those found in vivo. Descriptions of the in situ mechanical properties of aponeuroses are more common, but the results are variable. Our goal was to examine the mechanical properties of these tissues under conditions mimicking the in vivo state. Tissue strains were measured in the rat (Rattus norvegicus) soleus muscle directly from the spacing of metal markers implanted within the tissues of interest using an X-ray video microscope. Strains were measured for the tendon and three regions (proximal, middle and distal) of the aponeurosis. Muscle stimulation was accomplished through isolated ventral rootlets, allowing force to be graded in seven repeatable increments independent of muscle-tendon unit length. Peak strains (during maximal tetanic contraction at optimum length; Po) were ∼5% in tendon and ∼12% in all regions of the aponeurosis. At forces above 50% of Po, tissue stiffness was nearly constant in all regions, and a pronounced toe region was observed only at forces below ∼25% of Po. Stiffness increased in all regions as the muscle-tendon unit was lengthened. These results suggest that using mechanical properties measured ex vivo or during single contractile events in situ to estimate the in vivo behavior of tendon and aponeurosis may lead to errors in estimating the distribution of strain among the contractile and series elastic elements of the muscle.

Mechanical properties of the electrically silent adult rat soleus muscle

The isometric and isotonic in situ mechanical properties of the soleus muscle of adult female rats were determined after 60 days of inactivity induced by spinal cord isolation (SI). Compared to control, the absolute muscle mass, physiological cross‐sectional area, and maximum tetanic tension of the soleus in SI rats were reduced by 69%, 66%, and 77%, respectively. Isometric twitch time‐to‐peak‐tension and half‐relaxation times were 41% and 60% shorter in SI than control rats. The maximum velocity of shortening (mm/s), as determined using the afterloaded technique, was 66% faster in SI than control rats, whereas unloaded shortening velocity was similar in the two groups (9% faster in SI rats). Peak power was 48% lower in SI than control rats. The SI soleus was 39% more fatigable than control. Thus, the soleus became a smaller, faster, and more fatigable muscle following 60 days of inactivity. In general, the results indicate that the adaptations are of a lesser magnitude than those reported previously following denervation for the same duration. These data provide a baseline for future efforts to experimentally define the mechanisms of neurally mediated, but activity‐independent, regulation of the mechanical properties of the rat soleus muscle.

Does daily activity level determine muscle phenotype

SUMMARY The activation level of a muscle is presumed to be a major determinant of many mechanical and phenotypic properties of its muscle fibers. However, the relationship between the daily activation levels of a muscle and these properties has not been well defined, largely because of the lack of accurate and sustained assessments of the spontaneous activity levels of the muscle. Therefore, we determined the daily activity levels of selected rat hindlimb muscles using intramuscular EMG recordings. To allow comparisons across muscles having varying activity levels and/or muscle fiber type compositions, we recorded EMG activity in a predominantly slow plantarflexor (soleus), a predominantly fast plantarflexor (medial gastrocnemius, MG), a predominantly fast ankle dorsiflexor (tibialis anterior, TA) and a predominantly fast knee extensor (vastus lateralis, VL) in six unanesthetized rats for periods of 24 h. EMG activity levels were correlated with the light:dark cycle, with peak activity levels occurring during the dark period. The soleus was the most active and the TA the least active muscle in all rats. Daily EMG durations were highest for soleus (11–15 h), intermediate for MG (5–9 h) and VL (3–14 h) and lowest for TA (2–3 h). Daily mean EMG amplitudes and integrated EMG levels in the soleus were two- to threefold higher than in the MG and VL and seven- to eightfold higher than in the TA. Despite the three- to fourfold difference in activation levels of the MG and VL vs the TA, all three predominantly fast muscles have been reported to have a similar, very low percentage of slow fibers. Comparing these relative EMG levels to the published fiber type profiles of these muscles yields a very poor relationship between daily activity level and fiber type composition in the same muscles across several species. Although it is clear that changing the levels of activity can modulate the expression of the myosin phenotype, these results indicate that factors other than activation must play critical roles in determining and maintaining normal phenotypic properties of skeletal muscle fibers.

Is spinal cord isolation a good model of muscle disuse

The patterns of normal daily activity that are required to maintain normal skeletal muscle properties remain unknown. The present study was designed to determine whether spinal cord isolation can be used as a reliable experimental model of neuromuscular inactivity, that is, as a baseline for the absence of activity. Electromyograms (EMGs) were recorded from selected hindlimb muscles of unanesthetized rats over 24‐hour periods before and 7, 30, 60, and 90 days after surgical isolation of the lumbar spinal cord. Our data indicate that some rat slow muscle fibers pre‐surgery were activated for less than 3 hours per day. Spinal cord isolation (SI) reduced the mean daily integrated EMG (IEMG) and daily EMG duration in the primary slow extensor muscle (soleus) to <1% of control, and in the primary fast extensor muscles [medial gastrocnemius (MG) and vastus lateralis (VL)] to <2% of control. These parameters were decreased to <8% and 3% of control, respectively, in a primary fast flexor muscle, the tibialis anterior (TA). From 30 to 90 days post‐SI, the mean amplitudes of the spontaneous EMG bursts were relatively normal in the soleus, increased ∼2‐fold in the MG and VL, and increased ∼4‐fold in the TA. Some evidence of the normal antagonistic flexor–extensor relationship was apparent in the brief periods of recorded activity post‐SI. These results indicate that SI eliminates nearly all of the normal EMG activity in the hindlimb muscles in the presence of relatively normal muscle innervation and functional intraspinal neural circuitry. Muscle Nerve, 2006

Selectively reshaping a muscle phenotype: functional overload of cat plantaris.

Introduction: Functional overload (FO) of the fast plantaris muscle was studied in treadmill‐exercised (FO‐Ex) or sedentary (FO‐Sed) adult cats. Methods: Mechanical, phenotype, and kinematics analyses were performed. Results: Plantigrade vs. normal digitigrade posture was observed early post‐FO. Relative plantaris mass was greater in FO‐Sed (10%) and FO‐Ex (60%) cats than in controls 12 weeks post‐FO. Specific tension was similar across groups, indicating functional hypertrophy. Fiber size was greater, percent slow fibers higher, percent IIa myosin heavy chain (MHC) higher, and IIx MHC lower in FO‐Ex than controls. Twitch and half‐relaxation times were longer, and the frequency–tension curve shifted toward that observed in slow muscles. Electromyography (EMG) and tendon force amplitudes during stepping were larger, and the yield (lengthening) phase occurred at a longer muscle length before compared with after FO. Discussion: Reshaping the plantaris phenotype was highly dependent on the overload stimulus, indicating that electrical stimulation paradigms used during rehabilitation should be performed with the muscles under “loaded” conditions. Muscle Nerve, 2011