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Muscular hydrostats, such as octopus arms or elephant trunks, lack bones entirely, endowing them with exceptional dexterity and reconfigurability. Key to their unmatched ability to control nearly infinite degrees of freedom is the architecture into which muscle fibers are weaved. Their arrangement is, effectively, the instantiation of a sophisticated mechanical program that mediates, and likely facilitates, the control and realization of complex, dynamic morphological reconfigurations. Here, by combining medical imaging, biomechanical data, live behavioral experiments, and numerical simulations, an octopus-inspired arm made of $\sim$200 continuous muscle groups is synthesized, exposing “mechanically intelligent” design and control principles broadly pertinent to dynamics and robotics. Such principles are mathematically understood in terms of storage, transport, and conversion of topological quantities, effected into complex 3D motions via simple muscle activation templates. These are in turn composed into higher-level control strategies that, compounded by the arm’s compliance, are demonstrated across challenging manipulation tasks, revealing surprising simplicity and robustness. 

Squid use eight arms and two slender tentacles to capture prey. The muscular stalks of the tentacles are elongated approximately 80% in 20–40 ms towards the prey, which is adhered to the terminal clubs by arrays of suckers. Using a previously developed forward dynamics model of the extension of the tentacles of the squidDoryteuthis pealeii(formerlyLoligo pealeii), we predict how spatial muscle-activation patterns result in a distribution of muscular power, muscle work, and kinetic and elastic energy along the tentacle. The simulated peak extension speed of the tentacles is remarkably insensitive to delays of activation along the stalk, as well as to random variations in the activation onset. A delay along the tentacle of 50% of the extension time has only a small effect on the peak extension velocity of the tentacle compared with a zero-delay pattern. A slight delay of the distal portion relative to the proximal has a small positive effect on peak extension velocity, whereas negative delays (delay reversed along stalk) always reduce extension performance. In addition, tentacular extension is relatively insensitive to superimposed random variations in the prescribed delays along the stalk. This holds in particular for small positive delays that are similar to delays predicted from measured axonal diameters of motor neurons. This robustness against variation in the activation distribution reduces the accuracy requirements of the neuronal control and is likely due to the non-linear mechanical properties of the muscular tissue in the tentacle. 

ABSTRACT Obliquely striated muscles occur in 17+ phyla, likely evolving repeatedly, yet the implications of oblique striation for muscle function are unknown. Contrary to the belief that oblique striation allows high force output over extraordinary length ranges (i.e. superelongation), recent work suggests diversity in operating length ranges and length–force relationships. We hypothesize oblique striation evolved to increase length–force relationship flexibility. We predict that superelongation is not a general characteristic of obliquely striated muscles and instead that length–force relationships vary with operating length range. To test these predictions, we measured length–force relationships of five obliquely striated muscles from inshore longfin squid, Doryteuthis pealeii: tentacle, funnel retractor and head retractor longitudinal fibers, and arm and fin transverse fibers. Consistent with superelongation, the tentacle length–force relationship had a long descending limb, whereas all others exhibited limited descending limbs. The ascending limb at 0.6P0 was significantly broader (P<0.001) for the tentacle length–force relationship (0.43±0.04L0; where L0 is the preparation length that produced peak isometric stress, P0) than for the arm (0.29±0.03L0), head retractor (0.24±0.06L0), fin (0.20±0.04L0) and funnel retractor (0.27±0.03L0). The fin's narrow ascending limb differed significantly from those of the arm (P=0.004) and funnel retractor (P=0.012). We further characterized the tentacle preparation's maximum isometric stress (315±78 kPa), maximum unloaded shortening velocity (2.97±0.55L0 s−1) and ultrastructural traits (compared with the arm), which may explain its broader length–force relationship. Comparison of obliquely striated muscles across taxa revealed length–force relationship diversity, with only two species exhibiting superelongation.