In situmuscle power differs without varyingin vitromechanical properties in two insect leg muscles innervated by the same motor neuron

Abstract

The mechanical behavior of muscle during locomotion is often predicted by its anatomy, kinematics, activation pattern and contractile properties. The neuromuscular design of the cockroach leg provides a model system to examine these assumptions, because a single motor neuron innervates two extensor muscles operating at a single joint. Comparisons of the in situ measurements under in vivo running conditions of muscle 178 to a previously examined muscle (179) demonstrate that the same inputs (e.g. neural signal and kinematics) can result in different mechanical outputs. The same neural signal and kinematics, as determined during running, can result in different mechanical functions, even when the two anatomically similar muscles possess the same contraction kinetics, force-velocity properties and tetanic force-length properties. Although active shortening greatly depressed force under in vivo-like strain and stimulation conditions, force depression was similarly proportional to strain, similarly inversely proportional to stimulation level, and similarly independent of initial length and shortening velocity between the two muscles. Lastly, passive prestretch enhanced force similarly between the two muscles. The forces generated by the two muscles when stimulated with their in vivo pattern at lengths equal to or shorter than rest length differed, however. Overall, differences between the two muscles in their submaximal force-length relationships can account for up to 75% of the difference between the two muscles in peak force generated at short lengths observed during oscillatory contractions. Despite the fact that these muscles act at the same joint, are stimulated by the same motor neuron with an identical pattern, and possess many of the same in vitro mechanical properties, the mechanical outputs of two leg extensor muscles can be vastly different.

Dynamic properties of a locomotory muscle of the tobacco hornwormManduca sextaduring strain cycling and simulated natural crawling

“…A3 VIL, in contrast, dissipates most of the energy used to extend it, whether in sinusoidal strain cycling (Figs·4, 6) or during simulated natural crawling (Figs·11, 12), a property associated in locomotory structures of other organisms with maintenance of stability (Biewener and Roberts, 2000;Dudek and Full, 2006;Hof, 2003;Jindrich and Full, 2002;Marsh, 1999), by means of preflex rather than CNS-dependent reflex (Campbell and Kirkpatrick, 2001;Cham et al, 2000;Chen et al, 2006;Dickinson et al, 2000;Seipel et al, 2004). Although muscles of like mechanical qualities in vitro can have markedly different mechanical outputs in vivo (Ahn et al, 2006), the visual similarity of fibers in all M. sexta larval muscles at least raises the possibility that this low resilience may be a general characteristic of caterpillar muscles. Efficiency of caterpillar locomotion is very low (Casey, 1991), but given the growth-oriented role of the larval stage, locomotory efficiency may be unimportant; caterpillars allocate far more of their energy uptake to tissue production than to activity (Schowalter et al, 1977;Scriber, 1977).…”

Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain

“…The cockroach Blaberus discoidalis possesses a pair of dorsal/ventral femoral extensors 1 (178 and 179) (Carbonell, 1947) that are putative control muscles and innervated only by a single fast motor neuron (Df) (Pearson and Iles, 1971;Pipa and Cook, 1959). A single action potential in Df produces one, relatively large MAP in its target muscles, resulting in nearly identical patterns of activation in both extensors muscles (Ahn et al, 2006;Full et al, 1998;Watson and Ritzmann, 1995). When first recruited during running, these femoral extensors have been hypothesized to shorten the transition from flexion to extension and possibly increase joint angular velocity at higher speeds (Levi and Camhi, 1996;Watson and Ritzmann, 1998b).…”

A single muscle's multifunctional control potential of body dynamics for postural control and running

“…While correlating muscle activation changes and dynamics across a variety of perturbations can suggest causal relationships, and careful biomechanical models can offer potential explanations [25,[29][30][31], it is necessary to test these hypotheses with direct experimentation in the intact, behaving animal. This is especially true during dynamic behaviours where it is difficult to predict a muscle's function from anatomy alone or even a careful examination of its in situ physiological properties [16,32,33].…”