Neurons and molecules involved in noxious light sensation in Caenorhabditis elegans

Abstract

Ultraviolet (UV) light is a danger to unpigmented organisms, inducing photodamage of cells and DNA. The transparent nematode Caenorhabditis elegans, despite having no eyes, detects light and exhibits negative phototaxis in order to evade sunlight. UV absorption is detected by the photosensor protein LITE-1, that also responds to reactive oxygen species. We investigated which neurons express LITE-1 and act as noxious photosensors and how they transmit this sensation to the nervous system to evoke escape behavior. We identified the interneuron AVG as a main focus of LITE-1 function in mediating the noxious light evoked escape behavior, with minor roles of the interneuron PVT, the sensory ASK neurons and touch receptor neurons. AVG is activated by blue light, and also its optogenetic stimulation causes escape behavior. Signaling from AVG involves chemical neurotransmission, likely directly to premotor interneurons, and to other cells, by extrasynaptic signaling through the neuropeptide NLP-10. NLP-10 signaling is not required for the acute response, but for maintaining responsiveness to repeated noxious stimuli. The source of NLP-10 in this context is largely AVG, however, also other cells contribute, possibly PVT. This work uncovers entry points of sensory information to the neuronal circuits mediating behavioral responses to noxious UV/blue light. Article SummaryC. elegans senses noxious light and induces escape behavior to avoid damage. The photosensor protein LITE-1 mediates this sensation but understanding responsible neural circuits is incomplete. We identified neurons expressing LITE-1 and identify AVG as the main site of action. The neurotransmitter GABA plays a role in acuteness of the response. AVG, and other cells, need to release the neuropeptide NLP-10 to maintain responsiveness to repeated noxious stimuli. These findings help understanding the C. elegans photophobic response and will guide future work delineating the precise circuit pathways, as an example of how similar photosensation can evoke protective behavior in invertebrates.