Wake-like Skin Patterning and Neural Activity During Octopus Sleep

While sleeping, many vertebrate groups alternate between at least two sleep stages: rapid eye movement (REM) and slow wave sleep (SWS), in part characterized by wake-like and synchronous brain activity respectively. Sleep stage alternation has been implicated in learning and memory function experimentally1, and has motivated several techniques in training artificial neural networks2. If the functions ascribed to 2-stage sleep are truly general, one might expect to find similar phenomena outside the vertebrate lineage. Here we delineate neural and behavioral correlates of 2-stage sleep in octopuses, marine invertebrates which evolutionarily diverged from vertebrates ~550 MYA and have independently evolved large brains and behavioral sophistication. Octopus sleep is rhythmically interrupted by ~60 second bouts of pronounced body movements and rapid changes in their neurally controlled skin patterns. We show that this constitutes a distinct ‘active’ sleep stage, being homeostatically regulated, rapidly reversible, and coming with increased arousal threshold. Neuropixels recordings from the octopus central brain reveal that local field potential (LFP) activity during active sleep resembles that of waking. LFP activity differs across brain regions, with the strongest activity during active sleep seen in the Superior Frontal and Vertical lobes, anatomically connected regions associated with learning and memory function. During ‘quiet’ sleep, these regions are relatively silent but generate LFP oscillations resembling mammalian sleep spindles in frequency and duration. Computational analysis reveals the rich skin pattern dynamics of active sleep, which move through states strongly resembling waking skin patterns. The range of similarities with vertebrates implies that aspects of 2-stage sleep in octopuses may represent convergent features of complex cognition.