Sensory Glia Detect Repulsive Odorants and Drive Olfactory Adaptation

Glia are typically considered as supporting cells for neural development and synaptic transmission. Here, we report an active role of a glia in olfactory transduction. As a polymodal sensory neuron in C. elegans, the ASH neuron is previously known to detect multiple aversive odorants. We reveal that the AMsh glia, a sheath for multiple sensory neurons including ASH, cell-autonomously respond to aversive odorants via G-protein-coupled receptors (GPCRs) distinct from those in ASH. Upon activation, the AMsh glia suppress aversive odorant-triggered avoidance and promote olfactory adaptation by inhibiting the ASH neuron via GABA signaling. Thus, we propose a novel two-receptor model where the glia and sensory neuron jointly mediate adaptive olfaction. Our study reveals a non-canonical function of glial cells in olfactory transduction, which may provide new insights into the glia-like supporting cells in mammalian sensory procession. [Display omitted] •Both the AMsh glia and the ASH neurons cell-autonomously sense aversive odorants•SRH-79 and STR-61 function as the IAA receptors in AMsh glia and ASH, respectively•Upon activation, the AMsh glia promote olfactory adaptation by suppressing ASH•GABA mediates the AMsh glia-triggered neuronal suppression and olfactory adaptation Duan et al. report that a sheath glia cell-autonomously respond to aversive odorants. Upon activation, the glia suppress aversive odorants-triggered avoidance and promote olfactory adaptation by inhibiting neighboring olfactory neuron via GABA signaling. They propose a novel two-receptor model where the glia and sensory neuron jointly mediate adaptive olfaction.