Mechanics of a multiple muscle system: Intrinsic properties and in vivo performance of insect leg muscles

Presumed redundancy in a multiple muscle system may instead represent diversity in muscle function. The three hindlimb extensor muscles of the cockroach, Blaberus discoidalis, manage energy differently during running. I determined the in vivo strain and stimulation conditions of these three muscles during preferred speed running using electromyography and video-motion analysis techniques. Then, I isolated each muscle to measure its mechanical properties when operating under in vivo running conditions as well as the intrinsic mechanical properties under controlled stimulation and strain conditions. One muscle (177c) generates net mechanical energy, like a motor, during running. Muscle 177c is a relatively long muscle and shortens at one-third of its maximum contraction speed during running. Another muscle (178) both generates mechanical energy, like a motor, during stance, absorbs mechanical energy, like a brake, during swing. Over a stride, muscle 178 generates no net mechanical energy during running. A third muscle absorbs mechanical energy during running. Muscle 178 generates force during shortening, but also generates force during lengthening, to operate like both a motor during stance and a brake during swing. Muscle 179 does not generate force during the stance phase and only operates like a brake during the swing phase of running. Although muscles 178 and 179 are similar in length, contraction kinetics, maximum isometric force-length, maximum isometric force-velocity, force depression due to active shortening. Even when muscles 178 and 179 are stimulated and strained identically, muscle 178 generates mechanical energy and muscle 179 absorbs mechanical energy. A difference between the two muscles in their force-length relationships using their in vivo stimulation patterns and a difference in the amount force enhancement after a passive stretch could account for approximately 85% of the difference in peak force generated during oscillatory contractions. Using the in vivo conditions and examining the history-dependent properties of these muscles provide clues to how the muscles function differently during running. The locomotory muscles in an animal are constantly undergoing shortening and lengthening changes during cyclic behaviors such as running, flying and swimming. Understanding the functional consequences of shortening deactivation, stretch activation and submaximal stimulation can reveal differences of force generation that are not revealed during maximally stimulated, isometric and isotonic experiments.