Discovery of a body-wide photosensory array that matures in an adult-like animal and mediates eye-brain-independent movement and arousal.
Nishan ShettigarAnirudh ChakravarthySuchitta UmashankarVairavan LakshmananDasaradhi PalakodetiAkash GulyaniPublished in: Proceedings of the National Academy of Sciences of the United States of America (2021)
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.
Keyphrases
- low dose
- high throughput
- small molecule
- optical coherence tomography
- white matter
- high resolution
- optic nerve
- resting state
- oxidative stress
- young adults
- multiple sclerosis
- visible light
- cell proliferation
- intensive care unit
- cancer therapy
- functional connectivity
- signaling pathway
- extracorporeal membrane oxygenation
- blood brain barrier
- cell cycle arrest
- cerebral blood flow
- acute respiratory distress syndrome
- pi k akt
- light emitting
- childhood cancer