Non-uniformity of sarcomere lengths can explain the ?catch-like? effect of arthropod muscle

Abstract

The 'catch-like' effect, a hysteresis phenomenon in arthropod skeletal muscle contraction thought to be related to the catch of molluscan smooth muscle, was investigated in the closer muscle of the crab Eriphia spinifrons. Several parameters were varied to determine their influence on the catch-like effect. These parameters were (1) the frequency of repetitive stimulation of the slow excitatory neuron, (2) additional stimulation of the inhibitory neuron, (3) the amount of stretch applied to the muscle and (4) the stiffness of the mechano-electrical transducer. The results show that the catch-like effect is not related to the catch of molluscan smooth muscle but rather to the 'residual force enhancement' or 'creep' phenomenon described for vertebrate muscle. A hypothesis for residual force enhancement implies that the increase in force is caused by non-uniformity of sarcomere lengths along the muscle fibre. Based on this hypothesis and the actual force-length relationship of the crab muscle studied, calculations were carried out to determine, if the observed catch-like effect can be explained by such a model. The calculations corroborate the experimental evidence. The catch-like effect of arthropod muscles can thus be explained by the same mechanism responsible for residual force enhancement and creep in vertebrate muscle. A physiological relevance of the catch-like effect in arthropod muscle is inferred.

Maximum force production: why are crabs so strong?

“…It is well-known that crustaceans are able to generate higher maximum muscle stresses than vertebrates and most insects ( Josephson 1993). However, the physiological basis of this di¡erence has remained unresolved: are the higher stresses due simply to increases in the resting sarcomere length or is it necessary to invoke other ¢breassociated traits such as the density of the myosin ¢laments ( Jahromi & Atwood 1969;West et al 1992), arthropod`catch-like' e¡ects (GÏnzel & Rathmayer 1994), the myo¢brillar bundle diameter (Hilber & Galler 1998), di¡erences in the actin^myosin ¢lament ratios ( Jahromi & Atwood 1969;West et al 1992) and potential di¡erences in the actin^myosin cross-bridge duty factors (Cooke 1997)? Because of the heterogeneous nature of crustacean muscle (Atwood 1973) and because of the vast diversity of muscle types within the animal kingdom (Hoyle 1983), some have suggested that the sliding ¢lament model o¡ers little more than a general qualitative description of the relation between the structural features of muscle and performance ( Jahromi & Atwood 1969;Hoyle 1983).…”

Single perturbations cause sustained changes in searching behavior in stick insects

“…This effect describes the phenomenon that a short, high-frequency discharge of a motoneuron leads to a long-lasting increase in force production of a muscle that is maintained at a low frequency of motoneuron discharge. The effect has been described for crustacean muscles (Blaschko et al, 1931;Günzel and Rathmayer, The Journal of Experimental Biology 216 (6) 1994), locust tibial muscles (Wilson and Larimer, 1968) and the mesothoracic extensor tibiae in the stick insect Carausius morosus (Guschlbauer, 2009). If trochanteral muscles of stick insects possess catch-like properties, such an effect might hold the leg in the region of the PO.…”

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

“…This clearly differs from molluscan catch in that nerve stimulation and actomyosin activation occur throughout the contraction. The mechanism underlying this phenomenon is not well understood, although in one invertebrate case may arise in part from non-uniform sarcomere lengths (Günzel and Rathmayer, 1994).…”