Body-wide unique photoreceptor cells that allows head-removed flatworms to move like intact animals reveals the mechanistic framework underpinning one of the most sensitive eye–brain-independent responses known

Discovery of a body-wide photosensory array that matures in an adult-like animal and mediates eye–brain-independent movement and arousal. Nishan Shettigar, Anirudh Chakravarthy, Suchitta Umashankar, Vairavan Lakshmanan, Dasaradhi Palakodeti, and Akash Gulyani. Proceedings of the National Academy of Sciences, May 18, 2021 118 (20) e2021426118; https://doi.org/10.1073/pnas.2021426118

Popular version: https://www.nature.com/articles/d41586-021-01192-8

Significance: This study highlights the breathtaking sophistication of form and function possible with eye-independent light-sensory systems. We have discovered a body-wide sensory organization of unique photoreceptor cells that allows even head-removed flatworms to move like intact animals, revealing the mechanistic framework underpinning one of the most sensitive eye–brain-independent photoresponses known. Distinct from the ocular system, the body-wide sensory array matures in adult-like animals, can trigger arousal of intact animals from a “resting-state” and employs “noncanonical” opsins. Our discovery of a body-wide network of photoreceptor cells triggering coordinated movement is intriguing and conceptualizes how “dispersed”-sensory nodes may network to control outputs typically through a centralized brain. Our work illustrates how eye-independent systems can deeply influence animal physiology and behavior.

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.

Keywords: planariansextraocular photoreceptionUV-Aopsinslight-sensing