Proprioception in Muscle Hydrostats

Proprioception can be seen as a somatic sense stimulated by the action of the body itself. It is perceived through proprioceptors and is tightly linked to the animal body, as it is influenced by the biomechanical properties of the structures in which it is embedded. A specific class of these receptors, the muscle proprioceptors, project at several levels of the nervous system and provide information about limb position, whether in the presence or absence of movement, as well as muscle length, the sense of effort, and the sense of balance. In skeletal systems, proprioception is involved in postural maintenance, reflex actions, and rhythmic behaviors, but also in higher functions such as action planning and prediction. Proprioception can also be found in structures that are capable of movement without any real skeleton and are therefore called hydrostatic skeletons, both in humans and other animals. Hydrostatic bodies, including cephalopod limbs, the elephant trunk, and the human tongue, use muscle contractile forces to generate hydrostatic pressure, which acts as a skeleton to stabilize the structure and create motion. To provide online motion control of these bodies, the animal nervous system must cope with a huge amount of information coming from variables (such as length, angle, stiffness, and orientation) that continuously change throughout the entire structure. To limit this central burden, these structures may benefit from the presence of a muscle proprioceptive system used locally to control muscle contraction. Based on the current knowledge, many of the basic components of the proprioceptive system of soft-bodied and skeletal animals are essentially the same. Here, we aim to provide a forward-looking perspective on the role of muscle proprioception in motion, with a special focus on proprioception in muscular hydrostats. We wish to highlight the relevance of this topic across several fields of investigation, from human sensorimotor pathologies to soft robotics, where a high degree of autonomy in soft structures, combined with a reduced control demand, remains an unmet need. To address these gaps, we emphasize the need for improved knowledge and methodological assessment of this "sixth sense."