THE SIXTH SENSE OF THE OCTOPUS: THE USE OF PROPRIOCEPTION DURING MOTION

Proprioception is known as the ‘sixth sense’, as it provides information about body position and movement, and is therefore essential for motor control. The flexible arms of the octopus, with virtually unlimited degrees of freedom, evolved unique control strategy that enable fast stereotypical and reflex motions that do not require a brain-centred feedback control. In this study, we investigated the involvement and role of proprioception in the execution of such movements. Through proteomic and bioinformatic analysis, we first identified the presence of two Piezo-like mechanosensitive ion channel isoforms, X1 (A0A7E6FJ03) and X2 (A0A6P7TA58), in muscle tissue samples. Interestingly, immunofluorescence analysis revealed a regularly spaced distribution of Piezo-channels on the muscle cell membrane, localized in correspondence with calcium stores. We then performed step-stretch biomechanical experiments on arm muscle preparations, which showed the presence of stretch reflex response, a delayed increased in force following a rapid stretch, typical of proprioception-based responses. We show that this phenomenon is calcium-dependent and is reversibly blocked in the presence of GsMTx4, a known Piezo-channel blocker. We further identified the pathway of proprioception in whole-arm preparations with 3D reconstruction of the arm neural networks and electrophysiological recordings of the activity underlying stretch reflex. These experiments showed that proprioceptive inputs are transmitted to higher organizational levels of arm via a dense neuritic network. In conclusion, this study represents the first assessment of muscle proprioception function at lower-level control of the octopus arm and opens the way to further investigations into its role brain-centred complex motion.