Caterpillar Calisthenics Dynamics of a Slow, Stretchy Muscle During Strain Cycling and Simulated Natural Crawling

WOODS, W. A. Jr.*; FUSILLO, S. J. ; TRIMMER, B. A. ; Tufts University; Tufts University; Tufts University: Caterpillar Calisthenics: Dynamics of a Slow, Stretchy Muscle During Strain Cycling and Simulated Natural Crawling

Caterpillars are soft-bodied terrestrial climbers that accomplish a wide variety of complex movements with several hundred muscles and a relatively simple central nervous system. The muscles show some characteristics of supercontracting muscles, and during crawling cycle through strains up to 30% of resting length. We examined the ventral interior lateral muscle (VIL) of final instar Manduca sexta larvae. VIL contracts slowly, taking 1-1.5 s to reach tetanic peak force. In passive sinusoidal strain cycling over 20% of resting length, peak force was a log function of cycling frequency (r2 = 0.99), indicating viscoelasticity. After linear stretching from 90 to 110% of resting length, force immediately began to decay exponentially, with slower decay of force associated with slower lengthening; the time constant of the decay was a log function of strain rate for rates from 0.1 to 2 lengths s-1 (r2 = 0.94). Unlike insect wing muscles during flight, VIL does not undergo a sinusoidal strain cycle during crawling; rather, the muscle is at resting length for most of the cycle, with a linear shortening and re-lengthening occupying about 45% of cycle duration. EMG recordings show that VIL stimulation occurs at the initiation of shortening and ceases when the muscle is about 54% re-lengthened. In vitro preparations were subjected to strain cycling and stimulation similar to that of natural crawling. The stimulation phase, together with the slow development of force during stimulation, contribute to a clockwise work loop, indicating that during crawling VIL functions as a brake rather than as an actuator. The high working strain range, slow contraction, and viscoelastic properties of caterpillar muscle may be important elements of passive control during caterpillar locomotion.

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