How octopus arm muscle contractile properties and anatomical organization contribute to arm functional specialization.

Octopus arms are highly flexible structures capable of complex motions and are used in a wide repertoire of behaviors. Movements are generated by the coordinated summation of innervation signals to packed arrays of muscles oriented in different directions and moving based on their anatomical relationships. In this study, we investigated the interplay between muscle biomechanics and anatomical organization in the Octopus vulgaris arm to elucidate their role in different arm movements. We performed isometric and isotonic force measurements on isolated longitudinal and transverse arm muscles and showed that longitudinal muscles have a higher rate of activation and relaxation, lower twitch-to-tetanus ratio and lower passive tension than transverse muscles, thus prompting their use as faster and slower muscles, respectively. This points to the use of longitudinal muscles in more graded responses, such as those involved in precise actions, and transverse muscles in intense and sustained actions, such as motion stabilization and posture maintenance. Once activated, the arm muscles exert forces that cause deformations of the entire arm, which are determined by the amount, location, properties and orientation of their fibers. Here, we show that, although continuous, the arm manifests a certain degree of morphological specialization, where the arm muscles have a different aspect ratio along the arm. This possibly supports the functional specialization of arm portions observed in various motions, such as fetching and crawling. Hence, the octopus arm as a whole can be seen as a 'reservoir' of possibilities where different types of motion may emerge at the limb level through the co-option of the muscle contractile properties and structural arrangement.

Beyond muscles: role of intramuscular connective tissue elasticity and passive stiffness in octopus arm muscle function.

The octopus arm is a 'one of a kind' muscular hydrostat, as demonstrated by its high maneuverability and complexity of motions. It is composed of a complex array of muscles and intramuscular connective tissue, allowing force and shape production. In this study, we investigated the organization of the intramuscular elastic fibers in two main muscles composing the arm bulk: the longitudinal (L) and the transverse (T) muscles. We assessed their contribution to the muscles' passive elasticity and stiffness and inferred their possible roles in limb deformation. First, we performed confocal imaging of whole-arm samples and provided evidence of a muscle-specific organization of elastic fibers (more chaotic and less coiled in T than in L). We next showed that in an arm at rest, L muscles are maintained under 20% compression and T muscles under 30% stretching. Hence, tensional stresses are inherently present in the arm and affect the strain of elastic fibers. Because connective tissue in muscles is used to transmit stress and store elastic energy, we investigated the contribution of elastic fibers to passive forces using step-stretch and sinusoidal length-change protocols. We observed a higher viscoelasticity of L and a higher stiffness of T muscles, in line with their elastic fiber configurations. This suggests that L might be involved in energy storage and damping, whereas T is involved in posture maintenance and resistance to deformation. The elastic fiber configuration thus supports the specific role of muscles during movement and may contribute to the mechanics, energetics and control of arm motion.

The Diversity of Muscles and Their Regenerative Potential across Animals.

Cells with contractile functions are present in almost all metazoans, and so are the related processes of muscle homeostasis and regeneration. Regeneration itself is a complex process unevenly spread across metazoans that ranges from full-body regeneration to partial reconstruction of damaged organs or body tissues, including muscles. The cellular and molecular mechanisms involved in regenerative processes can be homologous, co-opted, and/or evolved independently. By comparing the mechanisms of muscle homeostasis and regeneration throughout the diversity of animal body-plans and life cycles, it is possible to identify conserved and divergent cellular and molecular mechanisms underlying muscle plasticity. In this review we aim at providing an overview of muscle regeneration studies in metazoans, highlighting the major regenerative strategies and molecular pathways involved. By gathering these findings, we wish to advocate a comparative and evolutionary approach to prompt a wider use of "non-canonical" animal models for molecular and even pharmacological studies in the field of muscle regeneration.