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

Proc Natl Acad Sci U S A. 2021 May 18;118(20):e2021426118. doi: 10.1073/pnas.2021426118.


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: UV-A; extraocular photoreception; light-sensing; opsins; planarians.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arousal / genetics
  • Arousal / physiology
  • Arousal / radiation effects
  • Brain / growth & development
  • Brain / metabolism*
  • Eye / growth & development
  • Eye / metabolism*
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Developmental
  • Helminth Proteins / classification
  • Helminth Proteins / genetics*
  • Helminth Proteins / metabolism
  • In Situ Hybridization, Fluorescence / methods
  • Locomotion / genetics
  • Locomotion / physiology
  • Locomotion / radiation effects
  • Movement / physiology
  • Movement / radiation effects
  • Opsins / classification
  • Opsins / genetics*
  • Opsins / metabolism
  • Photoreceptor Cells, Invertebrate / metabolism*
  • Phylogeny
  • Planarians / genetics*
  • Planarians / growth & development
  • Planarians / metabolism
  • RNA Interference
  • Ultraviolet Rays


  • Helminth Proteins
  • Opsins