The octopus arm hydrostatic limb: an efficient link between form and function

The Octopus vulgaris arm is a remarkable example of muscular hydrostat where extraordinary motor capabilities are achieved despite the absence of a rigid skeleton. The animal eight highly flexible arms exhibit a remarkable diversity and complexity of movements and can easily adapt to the surrounding environment. Indeed, unlike structures with rigid skeletal elements, whose movements are restricted to joints, in these arms, deformations such as bending, elongation, shortening, and twisting, can occur at any location and at multiple locations simultaneously. Furthermore, the octopus can vary the stiffness of its arms, transiently converting a flexible limb into a quasi-articulated structure to accomplish complex tasks like fetching objects and walking over the sea floor. For these reasons, for over a decades the octopus has been inspiring the design of flexible robotic arms and represents nowadays an “animal model” for soft robotics technologies. The octopus behavior and locomotion are achieved through the combination of basic stereotyped arm motions. At the arm level, this can be obtained by the selective activation or co-activation of antagonistic muscles. The aim of this thesis is to elucidate the bases of octopus arm behavioural flexibility investigating the arm structure to function relationship. Here we show that, while having a morphologically continuous structure, the arm presents behaviourally relevant morpho-functional regionalization, especially evident at the arm apical region. An additional level of flexibility in this system is achieved through the existence of transmural strain gradients generated by a decreasing waviness of elastic fibers from outer to the inner muscle layers determining a functional higher viscoelasticity of the outer muscle layers. This might be related with the distinct functions played by muscles during motions such as accommodation of strain of the inner muscle layers and storage and release elastic energy of the outer layers. This aspect might be important for the overall arm stabilization and compliance to deformation. In support of this data, we found differences in muscle activation properties wherefore inner layers behave as slow muscles and outer layers as fast muscles. Moreover, differently from vertebrates, hydrostatic muscles can undergo large deformations thus changing dramatically the strain rate of each muscle participating in the motion. In this scenario, an activation pattern from a given motorneuron can find the same muscle in a very different strain rate during the motion. Here we found that muscle strain rate has indeed a profound influence on its mechanical work output and, in conjunction with the activation pattern and mechanism of E-C coupling, this feature might be exploited by the animal to produce a wide spectrum of arm motion. Taken together these findings support the existence of a specific arrangement of highly coordinated muscles along and within the arm bulk that is consistent with the arm use. This study is particularly relevant to further implementation in computational models able not only to simulate natural arm movements but also to predict, through a reverse engineering approach, the motion outcome of muscle ensembles. Moreover, conveying the principles governing arm flexibility might have an important impact into the design and fabrication of bio-inspired flexible robotic arms endowed with high compliance and adaptability.