Discovery of a body-wide photosensory array that matures in an adult-like animal and mediates eye–brain-independent movement and arousal

Abstract

The ability to respond to light has profoundly shaped life. Animals with eyes overwhelmingly rely on their visual circuits for mediating light-induced coordinated movements. Building on previously reported behaviors, we report the discovery of an organized, eye-independent (extraocular), body-wide photosensory framework that allows even a head-removed animal to move like an intact animal. Despite possessing sensitive cerebral eyes and a centralized brain that controls most behaviors, head-removed planarians show acute, coordinated ultraviolet-A (UV-A) aversive phototaxis. We find this eye–brain-independent phototaxis is mediated by two noncanonical rhabdomeric opsins, the first known function for this newly classified opsin-clade. We uncover a unique array of dual-opsin–expressing photoreceptor cells that line the periphery of animal body, are proximal to a body-wide nerve net, and mediate UV-A phototaxis by engaging multiple modes of locomotion. Unlike embryonically developing cerebral eyes that are functional when animals hatch, the body-wide photosensory array matures postembryonically in “adult-like animals.” Notably, apart from head-removed phototaxis, the body-wide, extraocular sensory organization also impacts physiology of intact animals. Low-dose UV-A, but not visible light (ocular-stimulus), is able to arouse intact worms that have naturally cycled to an inactive/rest-like state. This wavelength selective, low-light arousal of resting animals is noncanonical-opsin dependent but eye independent. Our discovery of an autonomous, multifunctional, late-maturing, organized body-wide photosensory system establishes a paradigm in sensory biology and evolution of light sensing.

Quantification of planarian behaviors

“…24. Planarians respond to ultraviolet light through receptors existing at the surface throughout their body (Birkholz & Beane, 2017;Shettigar et al, 2021). Therefore, if planarian behaviors associated with eye-brain interaction are analyzed, ultraviolet light should be cut off (Figure 2a).…”

“…To measure the body size of living planarians, use graph paper placed under a Petri dish. It can easily be confirmed whether planarians are undergoing regeneration or have regenerated by confirming whether the pharynx is positioned at the middle of the body. Planarians respond to ultraviolet light through receptors existing at the surface throughout their body (Birkholz & Beane, 2017; Shettigar et al., 2021). Therefore, if planarian behaviors associated with eye‐brain interaction are analyzed, ultraviolet light should be cut off (Figure 2a).…”

Regeneration of Planarian Auricles and Reestablishment of Chemotactic Ability

“…This is also the case for planarian flatworms, free-living members of the phylum Platyhelminthes, which not only display chemotactic behavior, but also respond to differences in temperature, contact, light, and water flow (Miyamoto and Shimozawa, 1985;Umesono et al, 2011;Inoue et al, 2015;Inoue, 2017;Ross et al, 2018). Although planarians can respond to light of different wavelengths (Paskin et al, 2014;Shettigar et al, 2017;Shettigar et al, 2021), they are not known to detect shapes (Walter, 1907). The sensory systems of planarians are well-integrated with their central nervous system (Agata et al, 1998;Okamoto et al, 2005;Inoue et al, 2015).…”

Head removal enhances planarian electrotaxis

“…For example, it was shown that ciliary gliding depends on serotonergic signaling ( Currie and Pearson, 2013 ), that peristalsis and scrunching are distinct gaits ( Cochet-Escartin et al, 2015 ), with peristalsis resulting from non-functional cilia ( Rompolas et al, 2010 ) and scrunching being a cilia-independent escape gait ( Cochet-Escartin et al, 2015 ). Thermotaxis, phototaxis and chemotaxis have been found to require the presence of a brain to sense their respective stimuli ( Inoue et al, 2015 ), whereas fission ( Malinowski et al, 2017 ; Goel et al, 2021 ), scrunching ( Cochet-Escartin et al, 2015 ) and avoidance of local near-ultraviolet light stimulation ( Paskin et al, 2014 ; Shettigar et al, 2017 ; Le et al, 2021 ; Shettigar et al, 2021 ) can occur without a brain.…”