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

Abstract

ABSTRACT 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.