Sensory navigation results from coordinated transitions between distinct behavioral programs. During chemotaxis in the Drosophila melanogaster larva, the detection of positive odor gradients extends runs while negative gradients promote stops and turns. This algorithm represents a foundation for the control of sensory navigation across phyla. In the present work, we identified an olfactory descending neuron, PDM-DN, which plays a pivotal role in the organization of stops and turns in response to the detection of graded changes in odor concentrations. Artificial activation of this descending neuron induces deterministic stops followed by the initiation of turning maneuvers through head casts. Using electron microscopy, we reconstructed the main pathway that connects the PDM-DN neuron to the peripheral olfactory system and to the pre-motor circuit responsible for the actuation of forward peristalsis. Our results set the stage for a detailed mechanistic analysis of the sensorimotor conversion of graded olfactory inputs into action selection to perform goal-oriented navigation.

This work was initiated as part of the multi-lab Larval Olympiad conducted at the Janelia Research Campus. We are in debt to the work of S Reid (Louis lab) during the initial phase of the screen. We thank I Andrade, A Fushiki, J Jonaitis, I Larderet, P Schegel, C Schneider-Mizell and M Zwart for contributing to the EM reconstruction. We thank H Aberle for glutamate antibodies, as well as V Jayaraman, A Nern, S Pulver, G Rubin and J. Simpson for sharing fly lines. We thank V Jayaraman and R Francoville for training and access to the functional imaging setup. ML and DT acknowledges support of the Spanish Ministry of Economy and Competitiveness (MICINN and BFU2011-26208), ‘Centro de Excelencia Severo Ochoa 2013–2017’, the CERCA Programme/Generalitat de Catalunya, the EMBL/CRG Systems Biology Program and the University of California, Santa Barbara. IT was supported by the Marie Curie FP7 Programme through FLiACT (ITN). AK was supported by the ‘La Caixa’ International PhD Programme. JT, MZ and AC acknowledge funding from the Howard Hughes Medical Institute.