Use of Peripheral Sensory Information for Central Nervous Control of Arm Movement by Octopus vulgaris

Octopuses are active predators with highly flexible bodies and rich behavioral repertoires [1–3]. They display advanced cognitive abilities, and the size of their large nervous system rivals that of many mammals. However, only one third of the neurons constitute the CNS, while the rest are located in an elaborate PNS, including eight arms, each containing myriad sensory receptors of various modalities [2–4]. This led early workers to question the extent to which the CNS is privy to non-visual sensory input from the periphery and to suggest that it has limited capacity to finely control arm movement [3–5]. This conclusion seemed reasonable considering the size of the PNS and the results of early behavioral tests [3, 6–8]. We recently demonstrated that octopuses use visual information to control goal-directed complex single arm movements [9]. However, that study did not establish whether animals use information from the arm itself [9–12]. We here report on development of two-choice, single-arm mazes that test the ability of octopuses to perform operant learning tasks that mimic normal tactile exploration behavior and require the non-peripheral neural circuitry to use focal sensory information originating in single arms [1, 10]. We show that the CNS of the octopus uses peripheral information about arm motion as well as tactile input to accomplish learning tasks that entail directed control of movement. We conclude that although octopus arms have a great capacity to act independently, they are also subject to central control, allowing well-organized, purposeful behavior of the organism as a whole.