To avoid dangerous environments or maintain homeostasis, animals must constantly and reliably monitor key sensory modalities such as oxygen. Tonic sensory receptors can perceive such constant information but are not well understood. How are responses to sustained sensory signals generated, and how do they reconfigure neural circuits to change animal behaviour? I study the mechanisms underlying avoidance of high [O2] in C. elegans as a model for sustained homeostatic responses. Three head neurons and one tail neuron of C. elegans continuously respond to ambient O2. Tonic signalling in these neurons is sustained by calcium influx at the plasma membrane and also requires Ca2+ release from intracellular stores. Tonic signalling propagates to downstream neural circuits, including the hub interneuron RMG, to mediate oxygen responses. Interestingly, the tuning of these oxygen responses shows plasticity depending on experience, context, or genetic background.