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Muscles are multi-functional structures that interface neural and mechanical systems. Muscle work depends on a large multi-dimensional space of stimulus (neural) and strain (mechanical) parameters. In our companion paper, we rewrote activation to individual muscles in intact, behaving cockroaches (Blaberus discoidalisL.), revealing a specific muscle's potential to control body dynamics in different behaviours. Here, we use those results to provide the biologically relevant parameters forin situwork measurements. We test four hypotheses about how muscle function changes to provide mechanisms for the observed control responses. Under isometric conditions, a graded increase in muscle stress underlies its linear actuation during standing behaviours. Despite typically absorbing energy, this muscle can recruit two separate periods of positive work when controlling running. This functional change arises from mechanical feedback filtering a linear increase in neural activation into nonlinear work output. Changing activation phase again led to positive work recruitment, but at different times, consistent with the muscle's ability to also produce a turn. Changes in muscle work required considering the natural sequence of strides and separating swing and stance contributions of work. Bothin vivocontrol potentials andin situwork loops were necessary to discover the neuromechanical coupling enabling control.

SUMMARY In nature, cockroaches run rapidly over complex terrain such as leaf litter. These substrates are rarely rigid, and are frequently very compliant. Whether and how compliant surfaces change the dynamics of rapid insect locomotion has not been investigated to date largely due to experimental limitations. We tested the hypothesis that a running insect can maintain average forward speed over an extremely soft elastic surface (10 N m−1) equal to 2/3 of its virtual leg stiffness (15 N m−1). Cockroaches Blaberus discoidalis were able to maintain forward speed (mean ± s.e.m., 37.2±0.6 cm s−1 rigid surface versus 38.0±0.7 cm s−1 elastic surface; repeated-measures ANOVA, P=0.45). Step frequency was unchanged (24.5±0.6 steps s−1 rigid surface versus 24.7±0.4 steps s−1 elastic surface; P=0.54). To uncover the mechanism, we measured the animal's centre of mass (COM) dynamics using a novel accelerometer backpack, attached very near the COM. Vertical acceleration of the COM on the elastic surface had a smaller peak-to-peak amplitude (11.50±0.33 m s−2, rigid versus 7.7±0.14 m s−2, elastic; P=0.04). The observed change in COM acceleration over an elastic surface required no change in effective stiffness when duty factor and ground stiffness were taken into account. Lowering of the COM towards the elastic surface caused the swing legs to land earlier, increasing the period of double support. A feedforward control model was consistent with the experimental results and provided one plausible, simple explanation of the mechanism.