c– f, Relative to QS, AS bouts see an increase in eye movements ( c), body movements ( d), breathing rate (breaths per minute) ( e) and breathing variability (coefficient of variation) ( f). b, Recording mean skin brightness over longer timescales reveals rhythmic alternation between AS and QS. The top shows images of octopus body, viewed from the top with head facing up, from throughout the active bout. 2d–f).Ī, Mean skin brightness over time during an active rest bout. During the QS separating active bouts, animals generated brief (7.1 ± 0.3 s, n = 1,163 events, six animals) and subtle flashes of colouration with a rate that decreased over the time interval between active bouts (Fig. We quantified patterning behaviour using a convolutional neural network to segment nine animals from 1,743 h of video, tracking changes in the mean brightness of octopus skin (Fig. 1c,d) and increased breathing rate and arhythmicity (Fig. 1a,b and Supplementary Videos 1 and 2), accompanied by pronounced eye and body movements (Fig. Roughly every 60 min, this behaviour was interrupted by roughly 1-minute periods of rapid transitions through a series of skin patterns (Fig. We then examined neural activity and skin pattern dynamics during sleeping and waking, by developing new methods for behavioural recording and quantification, light-sheet imaging and LFP recordings using Neuropixels probes in these soft bodied animals.ĭuring daylight, nocturnal octopuses ( Octopus laqueus 22) closed their eyes, adopting a flat resting posture and a uniformly white skin pattern, previously described hallmarks of octopus quiet sleep (QS) 6, 17. Expanding on this previous work, we tested whether octopuses possess two stages of sleep behaviour. In octopus, this has been termed ‘active sleep’ (AS) and is accompanied by an increased arousal threshold, one of several criteria of sleep 15, 21. Sleeping cephalopods 17 have been observed to undergo rhythmic bouts of body twitches and rapid changes in skin patterning 6, 18, mediated by neural control of large populations of skin pigment cells (chromatophores) 19 among other specialized cell types 20. Octopuses are among the largest brained invertebrates and demonstrate a range of sophisticated behaviours 16, making them ideal for testing the generality of two-stage sleep. If the functions ascribed to two-stage sleep are truly general, then one may expect to find neural and behavioural correlates of two-stage sleep widely among animals showing complex cognitive abilities. Vertebrate rapid eye movements (REMs) and slow wave sleep are characterized by a core set of behavioural and electrophysiological correlates, and proposed cognitive functions 13, 14, 15 while showing a rich diversity of species-specific features 15. The range of similarities with vertebrates indicates that aspects of two-stage sleep in octopuses may represent convergent features of complex cognition. During quiet sleep, these regions are relatively silent but generate LFP oscillations resembling mammalian sleep spindles 11, 12 in frequency and duration. 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 7, 8, 9, 10. High-density electrophysiological recordings from the central brain reveal that the local field potential (LFP) activity during active sleep resembles that of waking. Computational analysis of active sleep skin patterning reveals diverse dynamics through a set of patterns conserved across octopuses and strongly resembling those seen while awake. We show that these bouts are homeostatically regulated, rapidly reversible and come with increased arousal threshold, representing a distinct ‘active’ sleep stage. ‘Quiet’ sleep in octopuses is rhythmically interrupted by approximately 60-s bouts of pronounced body movements and rapid changes in skin patterning and texture 6. 5) and have independently evolved large brains and behavioural sophistication. Here we delineate neural and behavioural correlates of two stages of sleep in octopuses, marine invertebrates that evolutionarily diverged from vertebrates roughly 550 million years ago (ref. While sleeping, many vertebrate groups alternate between at least two sleep stages: rapid eye movement and slow wave sleep 1, 2, 3, 4, in part characterized by wake-like and synchronous brain activity, respectively.
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