Drosophila epidermal cells are intrinsically mechanosensitive and drive nociceptive behavioral outputs
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Abstract
Somatosensory neurons (SSNs) that detect and transduce mechanical, thermal, and chemical stimuli densely innervate an animal’s skin. However, despite the fact that epidermal cells provide the first point of contact for sensory stimuli. our understanding of roles that epidermal cells play in SSN function, particularly nociception, remains limited. Here, we show that stimulating Drosophila epidermal cells elicits activation of SSNs including nociceptors and triggers a variety of behavior outputs, including avoidance and escape. Further, we find that epidermal cells are intrinsically mechanosensitive and that epidermal mechanically evoked calcium responses require the store-operated calcium channel Orai. Epidermal cell stimulation augments larval responses to acute nociceptive stimuli and promotes prolonged hypersensitivity to subsequent mechanical stimuli. Hence, epidermal cells are key determinants of nociceptive sensitivity and sensitization, acting as primary sensors of noxious stimuli that tune nociceptor output and drive protective behaviors.
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These results, along with the observation that rolling behaviors predominate the early behavioral responses to epidermal stimulation (Fig. 2B), suggest that the nervous system prioritizes nocifensive behavioral outputs following epidermal stimulation
While epidermal stimulation can broadly mediate SSN activity, how do you envision epidermal stimulation prioritizing nocifensive behavior? Does ensheathment of C4da and C3da neurons by epidermal cells explain the preferential response?
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C4da neurons, elicited nocifensive c-bending and/or rolling behaviors in 73% of larvae
This is an elegant and thorough study mechanistically describing the role of epidermal cells in regulating nociceptive behavior as well as SSN activity more broadly, in Drosophila. Congratulations on your beautiful work! I’m curious why direct optogenetic activation of epidermal cells leads to a similar fraction of larva bending relative to direct activation of nociceptors, versus less than half of larva rolling in response to direct activation of epidermal cells relative to direct activation of nociceptors?
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