From 100k pigment cells to skillful camouflage: the role of skin color changes in sleeping octopuses

Learning of a motor skill requires practice. Ample evidence suggests that ‘offline practice’ in the sleeping brains of animals, including humans, is crucial to any learning process. Offline practice allows for refining and consolidating neural activity pathways which are later executed during wake, which results in significant performance gains. However, in most animals, neural activity underlying offline practice is difficult to access and even more difficult to interpret. Therefore, the nature of neural activity underlying offline practice during sleep have remained elusive. Here, we study camouflage behavior in the octopus during wake and sleep. Octopuses possess the remarkable ability to rapidly modify pigment cells on their skin to match their highly visually complex environment. We combine high-resolution filming of their skin with electrophysiology recordings of their brain activity to capture the neural underpinnings of camouflage. Our theoretical framework captures the hierarchy of different spatial scales in the emergence of the octopus’ notable skin patterns and the dynamics of their transitions as they get reactivated on their skin during sleep. In addition, we bias the octopus experiences when awake to investigate the effect on the patterns’ reactivation during sleep. These findings elucidate how octopuses coordinate ~100k pigment cells to collectively give rise to highly intricate camouflage patterns, as well as the role of pattern reactivation during sleep.