A syntactic analysis of a complex motor action: the octopus arm ‘slap’

Abstract

The analysis of a natural motor action is always difficult, especially when different motor programs are combined within the same interaction with the environment. We analyzed the behavior of an octopus, Abdopus sp., filmed in tidal pools in Okinawa, Japan, which used the kinematic primitives of rotation and translation of its hydrostatic arms, and combined these kinematic behaviors serially and in parallel to ‘slap’ at fish in the wild. In total, 19 slaps were analyzed. The kinematics of arm movement were measured in both external and animal-centered reference frames, while the octopus was slapping at the fish. By combining these primitives, the octopus is able to maintain flexibility while controlling only a few degrees of freedom, a concept we term ‘flexible rigidity’. This slapping action supports Flash and Hochner’s embodied organization view of motor behavior, as well as their idea that motor primitives can combine syntactically to form a complex action. The octopus’s ability to use sensory feedback from the position of a moving fish target, along with the feed-forward motor primitives, allows for the building of complex actions at dynamic equilibrium with the environment. Over all, these findings lead to a more realistic view of how a complex behavior allows an animal to coordinate with its environment.