An adaptive transition from exploring the environment in search of vital resources to exploiting these resources once the search was successful is important to all animals. Here we study the neuronal circuitry that allows larval Drosophila melanogaster of either sex to negotiate this exploration-exploitation transition. We do so by combining Pavlovian conditioning with high-resolution behavioral tracking, optogenetic manipulation of individually identified neurons, and EM data-based analyses of synaptic organization. We find that optogenetic activation of the dopaminergic neuron DAN-i1 can both establish memory during training and acutely terminate learned search behavior in a subsequent recall test. Its activation leaves innate behavior unaffected, however. Specifically, DAN-i1 activation can establish associative memories of opposite valence after paired and unpaired training with odor, and its activation during the recall test can terminate the search behavior resulting from either of these memories. Our results further suggest that in its behavioral significance DAN-i1 activation resembles, but does not equal, sugar reward. Dendrogram analyses of all the synaptic connections between DAN-i1 and its two main targets, the Kenyon cells and the mushroom body output neuron MBON-i1, further suggest that the DAN-i1 signals during training and during the recall test could be delivered to the Kenyon cells and to MBON-i1, respectively, within previously unrecognized, locally confined branching structures. This would provide an elegant circuit motif to terminate search on its successful completion.

Amino acids are important nutrients for animals because they are necessary for protein synthesis in particular during growth, as well as for neurotransmission. However, little is known about how animals use past experience to guide their search for amino-acid-rich food. We reasoned that the larvae of Drosophila melanogaster are suitable for investigating this topic because they are the feeding and growth stages in the life cycle of these holometabolous insects. Specifically, we investigated whether experiencing an odour with a 20 amino-acid mixture as a semi-natural tastant during training establishes odourtastant associative memories. Across a broad concentration range (0.01-20 mmol l −1 ), such an amino-acid mixture was found to have a rewarding effect, establishing appetitive memory for the odour. To our surprise, however, manipulation of the test conditions revealed that relatively high concentrations of the amino-acid mixture (3.3 mmol l −1 and higher) in addition establish aversive memory for the odour. We then characterized both of these oppositely valenced memories in terms of their dependency on the number of training trials, their temporal stability, their modulation through starvation and the specific changes in locomotion underlying them. Collectively, and in the light of what is known about the neuronal organization of odour-food memory in larval D. melanogaster, our data suggest that these memories are established in parallel. We discuss the similarity of our results to what has been reported for sodium chloride, and the possible neurogenetic bases for concentration-dependent changes in valence when these tastants are used as reinforcers.