Regularly occurring bouts of retinal movements suggest an REM sleep-like state in jumping spiders

Abstract

Sleep and sleep-like states are present across the animal kingdom, with recent studies convincingly demonstrating sleep-like states in arthropods, nematodes, and even cnidarians. However, the existence of different sleep phases across taxa is as yet unclear. In particular, the study of rapid eye movement (REM) sleep is still largely centered on terrestrial vertebrates, particularly mammals and birds. The most salient indicator of REM sleep is the movement of eyes during this phase. Movable eyes, however, have evolved only in a limited number of lineages-an adaptation notably absent in insects and most terrestrial arthropods-restricting cross-species comparisons. Jumping spiders, however, possess movable retinal tubes to redirect gaze, and in newly emerged spiderlings, these movements can be directly observed through their temporarily translucent exoskeleton. Here, we report evidence for an REM sleep-like state in a terrestrial invertebrate: periodic bouts of retinal movements coupled with limb twitching and stereotyped leg curling behaviors during nocturnal resting in a jumping spider. Observed retinal movement bouts were consistent, including regular durations and intervals, with both increasing over the course of the night. That these characteristic REM sleep-like behaviors exist in a highly visual, long-diverged lineage further challenges our understanding of this sleep state. Comparisons across such long-diverged lineages likely hold important questions and answers about the visual brain as well as the origin, evolution, and function of REM sleep.

Keywords: dream; rapid eye movement; resting; salticid; sleep.

Fig. 1.

(A) Ethogram of a whole-night recording of a spiderling (E2108c, 09-03-2021 in the raw data). Colored boxes show observed behavioral sequences throughout the night. Green and purple lines show orientations of left and right retinal tube, respectively, extracted with automated video tracking (SI Appendix). Greyish blue shaded background areas indicate when the spider was not or only partially in dorsal view, limiting both manual and automated scoring of retinal movements (SI Appendix). (B) Screenshot from the video in A showing all tracked body points, with overlaid lines drawn from median lenses to the back of the retinal tubes. (C) Zoomed-in section of angular tracking overlaid on the manually scored retinal movements sequence highlighting the consistency between automated and manual scoring procedures. (D) Smoothed density plots showing durations (yellow) and intervals (gray) of retinal movement bouts. Black lines show medians. (E) Trajectory plots of left (green) and right (purple) ends of retinal tubes during 1 min of an REM sleep–like bout (Left) and 1 min of an in-between phase (Right; highlighted in C), with time progressing from dark to light shaded colors. (F) Example ethogram for an adult spider (E2102, 06-27-2021 in the raw data) showing regular periodicity of movement behaviors (twitching and leg curling).