A Glial Hub-and-Spoke Circuitry in C. elegans orchestrates bidirectional thermosensation.

Abstract

Thermosensation is evolutionarily conserved for survival, yet the roles of glia in temperature coding and circuit dynamics remain poorly understood. Here, we identify C. elegans AMsh glia as dual-mode thermosensory hubs that autonomously detect temperature fluctuations by co-expressing the heat receptor GCY-28 (guanylate cyclase) and cold receptor GLR-3 (ionotropic glutamate receptor). Thermal changes induce spatiotemporal calcium dynamics in glia, driving GABA release to bidirectionally modulate neural circuits: enhancing AFD-mediated warmth detection through the excitatory receptor EXP-1 and suppressing ASH-dependent cold avoidance via the inhibitory receptor LGC-38. This GABAergic hub-and-spoke architecture regulates a broad range of thermal behaviors, including thermal avoidance, thermal resistance, and thermal preference. These findings establish glia as critical interpreters of environmental cues, highlighting their dual roles as sensors and modulators in sensory processing and providing a paradigm for understanding conserved glial mechanisms in neural circuit dynamics and behavioral plasticity.