Converging Circuits Mediate Temperature and Shock Aversive Olfactory Conditioning in Drosophila

Drosophila learn to avoid odors that are paired with aversive stimuli. Electric shock is a potent aversive stimulus that acts via dopamine neurons to elicit avoidance of the associated odor. While dopamine signaling has been demonstrated to mediate olfactory electric shock conditioning, it remains unclear how this pathway is involved in other types of behavioral reinforcement, such as in learned avoidance of odors paired with increased temperature. To better understand the neural mechanisms of distinct aversive reinforcement signals, we here established an olfactory temperature conditioning assay comparable to olfactory electric shock conditioning. We show that the AC neurons, which are internal thermal receptors expressing dTrpA1, are selectively required for odor-temperature but not for odor-shock memory. Furthermore, these separate sensory pathways for increased temperature and shock converge onto overlapping populations of dopamine neurons that signal aversive reinforcement. Temperature conditioning appears to require a subset of the dopamine neurons required for electric shock conditioning. We conclude that dopamine neurons integrate different noxious signals into a general aversive reinforcement pathway. •We established a temperature learning paradigm compatible to odor-shock learning•dTrpA1-expressing AC neurons are required for temperature, but not shock, conditioning•Dopamine neurons integrate aversive reinforcement of both temperature and shock•Dopamine neurons for temperature reinforcement are a subset of those for shock Galili et al. show that two aversive stimuli, electric shock and high temperature, are received by distinct sensory neurons in Drosophila, but the neuronal signals converge onto the same dopamine neurons to represent negative values. High temperature is received via dTRPA1 in internal sensor cells, AC neurons, and conveyed to the dopamine neurons.