Neural Control and Biomechanics of the Octopus Arm Muscular Hydrostat

Octopus vulgaris is a cephalopod mollusk with outstanding motor capabilities, built upon the action of eight soft and exceptionally flexible appendages. In the absence of any rigid skeletal-like support, the octopus arm works as a “muscular hydrostat” and movement is generated from the antagonistic action of two main muscle groups (longitudinal, L, and transverse, T, muscles) under an isovolumetric constrain. This peculiar anatomical organization evolved along with novel morphological arrangements, biomechanical properties, and motor control strategies aimed at reducing the computational burden of controlling unconstrained appendages endowed with virtually infinite degrees of freedom of motion. Hence, the octopus offers the unique opportunity to study a motor system, different from those of skeletal animals, and capable of controlling complex and precise motor tasks of eight arms with theoretically infinite degrees of freedom. Here, we investigated the octopus arm motor system employing a bottom-up approach. We began by identifying the motor neuron population and characterizing their organization in the arm nervous system. We next performed an extensive biomechanical characterization of the arm muscles focusing on the morphofunctional properties that are likely to facilitate the dynamic deformations occurring during arm movement. We show that motor neurons cluster in specific regions of the arm ganglia following a topographical organization. In addition, T muscles exhibit biomechanical properties resembling those of vertebrate slow muscles whereas L muscles are closer to those of vertebrate fast muscles. This difference is enhanced by the hydrostatic pressure inherently present in the arm, which causes the two muscles to operate under different conditions. Interestingly, these features underlie the different use of arm muscles during specific tasks Thus, the octopus evolved several arm-embedded adaptations to reduce the motor control complexity and increase the energetic efficiency of arm motion. This study find relevance also in the blooming field of soft-robotics. Indeed, an increasing number of researchers are currently aiming to design and construct bio-inspired soft-robotic manipulators, more flexible and versatile than their “hard” counterparts and more suited to perform gentle tasks and to interact with biological tissues. In this context, the octopus emerged as a pivotal source of inspiration for motor control principles underlying motion in soft-bodied limbs.