Specific Ion Channels Control Sensory Gain, Sensitivity, and Kinetics in a Tonic Thermonociceptor

• Published in: Cell reports (Cambridge) 2020-01, Vol.30 (2), p.397-408.e4
• Main Authors: Saro, Gabriella, Lia, Andrei-Stefan, Thapliyal, Saurabh, Marques, Filipe, Busch, Karl Emanuel, Glauser, Dominique A.
• Format: Article
• Language: English
• Subjects: Animals; Animals, Genetically Modified; Caenorhabditis elegans; cold sensation; heat sensation; Ion Channels - metabolism; NALCN; Nociceptors - metabolism; optogenetics; Optogenetics - methods; RyR; Temperature; thermosensation; Thermosensing - physiology; TRP; VGCC
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2019.12.029

Pain sensation and aversive behaviors entail the activation of nociceptor neurons, whose function is largely conserved across animals. The functional heterogeneity of nociceptors and ethical concerns are challenges for their study in mammalian models. Here, we investigate the function of a single type of genetically identified C. elegans thermonociceptor named FLP. Using calcium imaging in vivo, we demonstrate that FLP encodes thermal information in a tonic and graded manner over a wide thermal range spanning from noxious cold to noxious heat (8°C–36°C). This tonic-signaling mode allows FLP to trigger sustained behavioral changes necessary for escape behavior. Furthermore, we identify specific transient receptor potential, voltage-gated calcium, and sodium “leak” channels controlling sensory gain, thermal sensitivity, and signal kinetics, respectively, and show that the ryanodine receptor is required for long-lasting activation. Our work elucidates the task distribution among specific ion channels to achieve remarkable sensory properties in a tonic thermonociceptor in vivo. [Display omitted] •FLP neurons are nonadapting tonic thermonociceptors in C. elegans•FLPs encode absolute temperature rather than thermal changes•Multiple ion channels orchestrate thermosensory encoding by FLP•FLPs mediate both phasic and tonic behavioral responses Saro et al. ask how sensory information is encoded in a tonic thermonociceptor neuron. The work highlights a distribution of tasks among different ion channels controlling the detection, amplification, stabilization, and termination of signals and reveals the importance of their orchestration to control short- and long-term aversive behaviors.