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Different interoceptive systems must be integrated to ensure that multiple homeostatic insults evoke appropriate behavioral and physiological responses. Little is known about how this is achieved. Using  C. elegans , we dissect cross-modulation between systems that monitor temperature, O 2  and CO 2 . CO 2  is less aversive to animals acclimated to 15°C than those grown at 22°C. This difference requires the AFD neurons, which respond to both temperature and CO 2  changes. CO 2  evokes distinct AFD Ca 2+  responses in animals acclimated at 15°C or 22°C. Mutants defective in synaptic transmission can reprogram AFD CO 2  responses according to temperature experience, suggesting reprogramming occurs cell autonomously. AFD is exquisitely sensitive to CO 2 . Surprisingly, gradients of 0.01% CO 2 /second evoke very different Ca 2+  responses from gradients of 0.04% CO 2 /second. Ambient O 2  provides further contextual modulation of CO 2  avoidance. At 21% O 2  tonic signalling from the O 2 -sensing neuron URX inhibits CO 2  avoidance. This inhibition can be graded according to O 2  levels. In a natural wild isolate, a switch from 21% to 19% O 2  is sufficient to convert CO 2  from a neutral to an aversive cue. This sharp tuning is conferred partly by the neuroglobin GLB-5. The modulatory effects of O 2  on CO 2  avoidance involve the RIA interneurons, which are post-synaptic to URX and exhibit CO 2 -evoked Ca 2+  responses. Ambient O 2  and acclimation temperature act combinatorially to modulate CO 2  responsiveness. Our work highlights the integrated architecture of homeostatic responses in  C. elegans .

Cross-Modulation of Homeostatic Responses to Temperature, Oxygen and Carbon Dioxide in C. elegans