Individual bitter-sensing neurons in Drosophila exhibit both ON and OFF responses that influence synaptic plasticity

Abstract

The brain creates internal representations that translate sensory stimuli into appropriate behavior. Most studies of sensory processing focus on which subsets of neurons are activated by a stimulus, but the temporal features of the neural response are also important for behavior. In the taste system, the timing of peripheral sensory responses has rarely been examined. We investigated the temporal properties of taste responses in Drosophila melanogaster and discovered that different types of taste sensory neurons show striking differences in their response dynamics. Strong responses to stimulus onset (ON responses) and offset (OFF responses) were observed in bitter-sensing neurons in the labellum, whereas bitter neurons in the leg and other classes of labellar taste neurons showed only an ON response. Individual bitter labellar neurons generate both the ON and OFF responses through a cell-intrinsic mechanism that requires canonical bitter receptors. The bitter ON and OFF responses at the periphery are propagated to dopaminergic neurons that innervate the mushroom body and mediate aversive learning. When bitter is used as a reinforcement cue, the bitter ON and OFF responses can drive opposing types of synaptic plasticity and the effect of the OFF response dominates, likely due to the rapid and preferential habituation of the ON response. Together, these studies characterize novel features of neural responses in the taste system and reveal their importance for neural circuit function.