All animals rely on their ability to sense and respond to their environment to survive. While similar signal transduction pathways are implicated in both C. elegans and vertebrate chemosensation, there are still large gaps in our understanding of the mechanisms used to regulate signaling in these systems. In my thesis, I have identified a new role for the C. elegans cGMP-dependent protein kinase (PKG) EGL-4 in the negative regulation of nociceptive chemosensory signaling. Nociceptive sensory systems detect harmful stimuli and allow for the initiation of protective behavioral responses. The polymodal ASH sensory neurons are the primary nociceptors in C. elegans. The data suggest that EGL-4 negatively regulates signaling and behavior by activating known inhibitors of G protein-coupled signal transduction, RGS proteins. Using C. elegans behavioral response to aversive stimuli as the readout for neuronal activity, I provide the first evidence for PKG regulation of RGS function in sensory neurons in any system. Additionally, the suitability of a behavioral response is context-dependent, and must reflect both an animal's life history and its present internal state. Based on the integration of these variables, an animal's needs can be prioritized to optimize survival strategies. I show that cGMP movement through a gap junction neural network allows dynamic repurposing of several C. elegans head sensory neurons to regulate ASH sensitivity through EGL-4 function in response to an animal's feeding status. Such decentralized regulation of ASH signaling allows for rapid correlation between an animal's internal state and its behavioral output, and lends an unexpected modulatory flexibility to this hard-wired nociceptive neural circuit.