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Past work has shown that chronic exposure ofDrosophilato intense monomolecular odors in early life leads to homeostatic adaptation of olfactory neural responses and behavioral habituation to the familiar odor. Here, we found that, in contrast, persistent exposure to natural odors in early life increases behavioral attraction selectively to familiar odors. Odor experience increases the attractiveness of natural odors that are innately attractive and decreases the aversiveness of natural odors that are innately aversive. These changes in olfactory behavior are unlikely to arise from changes in the sensitivity of olfactory neurons at the first stages of olfactory processing: odor-evoked output from antennal lobe projection neurons was unchanged by chronic exposure to natural odors in terms of olfactory sensitivity, relational distances between odors, or response dynamics. We reveal a requirement for additional features of the environment beyond the odor in establishing odor experience-dependent behavioral plasticity. Passive odor exposure in a featureless environment lacking strong reinforcing cues was insufficient to elicit changes in olfactory preference; however, the same odor exposure resulted in behavioral plasticity when food was present in the environment. Together, these results indicate that behavioral plasticity elicited by persistent exposure to natural odors in early life is mediated by an associative process. In addition, they highlight the importance of using naturalistic odor stimuli for investigating olfactory function.

Animal brains use the relative timing between sensory cues and behaviorally salient events to form predictive associations about their environment. Handler and colleagues provide new mechanistic insights into how differential signaling downstream of dopamine receptors couples this timing to the dynamic reweighting of synapses that link sensation to action.

Dopaminergic neurons (DANs) signal punishment and reward during associative learning. In mammals, DANs show associative plasticity that correlates with the discrepancy between predicted and actual reinforcement (prediction error) during classical conditioning. Also in insects, such as Drosophila, DANs show associative plasticity that is, however, less understood. Here, we study associative plasticity in DANs and their synaptic partners, the Kenyon cells (KCs) in the mushroom bodies (MBs), while training Drosophila to associate an odorant with a temporally separated electric shock (trace conditioning). In most MB compartments DANs strengthened their responses to the conditioned odorant relative to untrained animals. This response plasticity preserved the initial degree of similarity between the odorant- and the shock-induced spatial response patterns, which decreased in untrained animals. Contrary to DANs, KCs (α'/β'-type) decreased their responses to the conditioned odorant relative to untrained animals. We found no evidence for prediction error coding by DANs during conditioning. Rather, our data supports the hypothesis that DAN plasticity encodes conditioning-induced changes in the odorant's predictive power.

Summary Background 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. Results 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. Conclusions We conclude that dopamine neurons integrate different noxious signals into a general aversive reinforcement pathway.

Trace conditioning is a form of associative learning that can be induced by presenting a conditioned stimulus (CS) and an unconditioned stimulus (US) following each other, but separated by a temporal gap. This gap distinguishes trace conditioning from classical delay conditioning, where the CS and US overlap. To bridge the temporal gap between both stimuli and to form an association between CS and US in trace conditioning, the brain must keep a neural representation of the CS after its termination—a stimulus trace. Behavioral and physiological studies on trace and delay conditioning revealed similarities between the two forms of learning, like similar memory decay and similar odor identity perception in invertebrates. On the other hand differences were reported also, like the requirement of distinct brain structures in vertebrates or disparities in molecular mechanisms in both vertebrates and invertebrates. For example, in commonly used vertebrate conditioning paradigms the hippocampus is necessary for trace but not for delay conditioning, and Drosophila delay conditioning requires the Rutabaga adenylyl cyclase (Rut-AC), which is dispensable in trace conditioning. It is still unknown how the brain encodes CS traces and how they are associated with a US in trace conditioning. Insects serve as powerful models to address the mechanisms underlying trace conditioning, due to their simple brain anatomy, behavioral accessibility and established methods of genetic interference. In this review we summarize the recent progress in insect trace conditioning on the behavioral and physiological level and emphasize similarities and differences compared to delay conditioning. Moreover, we examine proposed molecular and computational models and reassess different experimental approaches used for trace conditioning.