Shortening deactivation: quantifying a critical component of cyclical muscle contraction

A muscle undergoing cyclical contractions requires fast and efficient muscle activation and relaxation to generate high power with relatively low energetic cost. To enhance activation and increase force levels during shortening, some muscle types have evolved stretch activation (SA), a delayed increased in force following rapid muscle lengthening. SA's complementary phenomenon is shortening deactivation (SD), a delayed decrease in force following muscle shortening. SD increases muscle relaxation, which decreases resistance to subsequent muscle lengthening. While it might be just as important to cyclical power output, SD has received less investigation than SA. To enable mechanistic investigations into SD and quantitatively compare it to SA, we developed a protocol to elicit SA and SD from Drosophila and Lethocerus indirect flight muscles (IFM) and Drosophila jump muscle. When normalized to isometric tension, Drosophila IFM exhibited a 118% SD tension decrease, Lethocerus IFM dropped by 97%, and Drosophila jump muscle decreased by 37%. The same order was found for normalized SA tension: Drosophila IFM increased by 233%, Lethocerus IFM by 76%, and Drosophila jump muscle by only 11%. SD occurred slightly earlier than SA, relative to the respective length change, for both IFMs; but SD was exceedingly earlier than SA for jump muscle. Our results suggest SA and SD evolved to enable highly efficient IFM cyclical power generation and may be caused by the same mechanism. However, jump muscle SA and SD mechanisms are likely different, and may have evolved for a role other than to increase the power output of cyclical contractions.

Effects of muscle shortening on single-fiber, motor unit, and compound muscle action potentials

Even under isometric conditions, muscle contractions are associated with some degree of fiber shortening. The effects of muscle shortening on extracellular electromyographic potentials have not been characterized in detail. Moreover, the anatomical, biophysical, and detection factors influencing the muscle-shortening effects have been neither identified nor understood completely. Herein, we investigated the effects of muscle shortening on the amplitude and duration characteristics of single-fiber, motor unit, and compound muscle action potentials. We found that, at the single-fiber level, two main factors influenced the muscle-shortening effects: (1) the electrode position and distance relative to the myotendinous zone and (2) the electrode distance to the maxima of the dipole field arising from the stationary dipole created at the fiber-tendon junction. Besides, at the motor unit and muscle level, two additional factors were involved: (3) the overlapping between the propagating component of some fibers with the non-propagating component of other fibers and (4) the spatial spreading of the fiber-tendon junctions. The muscle-shortening effects depend critically on the electrode longitudinal distance to the myotendinous zone. When the electrode was placed far from the myotendinous zone, muscle shortening resulted in an enlargement and narrowing of the final (negative) phase of the potential, and this enlargement became less pronounced as the electrode approached the fiber endings. For electrode locations close to the myotendinous zone, muscle shortening caused a depression of both the main (positive) and final (negative) phases of the potential. Beyond the myotendinous zone, muscle shortening led to a decrease of the final (positive) phase. The present results provide reference information that will help to identify changes in MUPs and M waves due to muscle shortening, and thus to differentiate these changes from those caused by muscle fatigue. Graphical abstract

Plantar flexor muscles of kangaroo rats (D. deserti) shorten at a velocity to produce optimal power during jumping

During jumping by kangaroo rats, the musculotendon work contributions across all joints are not well understood. Namely, measures of external joint work do not provide information on the contributions from individual muscles or in-series elastic structures. In this study, we examined the functional roles of a major ankle extensor muscle, lateral gastrocnemius (LG), and of a major knee extensor muscle, vastus lateralis (VL), through in vivo sonomicrometry and electromyography techniques, during vertical jumping by kangaroo rats. Our data showed that both muscles increased shortening and activity with higher jumps. We found that knee angular velocity and VL muscle shortening velocity were coupled in time. In contrast, the ankle angular velocity and LG muscle shortening velocity were decoupled, and rapid joint extension near the end of the jump produced high power outputs at the ankle joint. Further, the decoupling of muscle and joint kinematics allowed the LG muscle to prolong the period of shortening velocity near optimal velocity (Vopt), which likely enabled the muscle to sustain maximal power generation. These observations were consistent with a LG tendon that is much more compliant than that of the VL.

Anconeus motor unit firing rates during isometric and muscle-shortening contractions comparing young and very old adults

Changes of neural drive to the muscle with adult aging, measured as motor unit firing rates during limb movements, are unknown. Throughout maximal voluntary efforts we found that, in comparison with young adults, firing rates were lower during isometric contraction in older adults but not different during elbow extension movements. Despite the older group being ∼33% weaker across contractions, their muscles can receive neural drive during movements that are similar to that of younger adults.

Positive end-expiratory pressure affects geometry and function of the human diaphragm

We demonstrate that PEEP causes changes in diaphragm geometry, especially muscle shortening, and decreases in vivo diaphragm contractile function. Thus prerequisites for the development of diaphragm longitudinal muscle atrophy are present with the acute application of PEEP. Once confirmed in ventilated critically ill patients, this could provide a new mechanism for ventilator-induced diaphragm dysfunction and ventilator weaning failure in the intensive care unit (ICU).

Tongue Muscle Anatomy: Architecture and Function

The tongue is composed entirely of soft tissue: muscle, fat, and connective tissue. This unusual composition and the tongue’s 3D muscle fiber orientation result in many degrees of freedom. The lack of bones and cartilage means that muscle shortening creates deformations, particularly local deformations, as the tongue moves into and out of speech gestures. The tongue is also surrounded by the hard structures of the oral cavity, which both constrain its motion and support the rapid small deformations that create speech sounds. Anatomical descriptors and categories of tongue muscles do not correlate with tongue function as speech movements use finely controlled co-contractions of antagonist muscles to move the oral structures during speech. Tongue muscle volume indicates that four muscles, the genioglossus, verticalis, transversus, and superior longitudinal, occupy the bulk of the tongue. They also comprise a functional muscle grouping that can shorten the tongue in the x, y, and z directions. Various 3D muscle shortening patterns produce large- or small-scale deformations in all directions of motion. The interdigitation of the tongue’s muscles is advantageous in allowing co-contraction of antagonist muscles and providing nimble deformational changes to move the tongue toward and away from any position.