A neural circuit mechanism for food odor perception and appetitive arousal in drosophila larvae
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The sense of smell is crucial to animals for providing external information about food properties and quality, potential threats and pleasure. Odors induce various emotional or cognitive responses which trigger behavior activities. However, understanding how olfactory inputs are perceived by cognitive processing centers and translates into behavior outputs remains challenging. Due to their simple nervous systems and stereotyped olfactory driven behavior, Drosophila larvae constitute a well-established model for studying odor representation, odor perception and odor driven behaviors. Here, we found that after brief exposure to appetitive odorants, 3rd instar fed larvae display feeding rate increase on sugar-rich food. We identified four appetitive odor-responsive dopaminergic neurons (DL2) as a third order olfactory neurons. Activation of those DL2 dopamine neurons mimics the appetitive feeding effect of odor stimulation. Furthermore, we showed that neuropeptide F(NPF), a neuropeptide Y-like neuromodulator and its receptor NPFR1 mediate a gating mechanism for reception of olfactory inputs in DL2 neurons. Drosophila larvae also display selective recognition of food related odors, indicated as an inverted U function: doses either too high or too low are not appetitive. We found that the four DL2 DA neurons combinatorially integrate olfactory inputs into one dimensional DA signals. The intensity of odor stimuli to DL2 neurons positively regulates DA signal outputs. Then, those odor-induced DA signals relay to downstream target neurons which express D1-like receptor Dop1R1 and NPF. Furthermore, an ensemble of Dop1R1 and its effectors play two functional roles: 1) A Dop1R1/G13F/Irk2-mediated inhibitory effect on the NPF neurons when strong odor stimuli trigger excessive release of odor-evoked DA signals, 2) A Dop1R1/Gαs-mediated default excitatory mechanism that mediates NPF neuronal response to any odor stimuli that are at or above the minimal threshold strength. Thus, through this tuning mechanism, Dop1R1 precisely restrict NPF neuronal response to a narrow range of odor-evoked DA signals levels. Overall, we have developed a novel behavioral paradigm using Drosophila larvae to investigate reception and processing of appetitive olfactory inputs in higher-order olfactory centers, as well as how food related olfactory cues are precisely perceived in downstream reward systems to trigger appetitive behavior output. Our findings may provide a general understanding of molecular and cellular mechanisms underlying DA-modulated appetitive odor perception and odor induced reward anticipation.