title: Olfactory neuromodulation of motion vision circuitry in Drosophila.
abstract: It is well established that perception is largely multisensory; often served by modalities such as touch, vision, and hearing that detect stimuli emanating from a common point in space; and processed by brain tissue maps that are spatially aligned. However, the neural interactions among modalities that share no spatial stimulus domain yet are essential for robust perception within noisy environments remain uncharacterized. Drosophila melanogaster makes its living navigating food odor plumes. Odor acts to increase the strength of gaze-stabilizing optomotor reflexes to keep the animal aligned within an invisible plume, facilitating odor localization in free flight. Here, we investigate the cellular mechanism for cross-modal behavioral interactions. We characterize a wide-field motion-selective interneuron of the lobula plate that shares anatomical and physiological similarities with the "Hx" neuron identified in larger flies. Drosophila Hx exhibits cross-modal enhancement of visual responses by paired odor, and presynaptic inputs to the lobula plate are required for behavioral odor tracking but are not themselves the target of odor modulation, nor is the neighboring wide-field "HSE" neuron. Octopaminergic neurons mediating increased visual responses upon flight initiation also show odor-evoked calcium modulations and form connections with Hx dendrites. Finally, restoring synaptic vesicle trafficking within the octopaminergic neurons of animals carrying a null mutation for all aminergic signaling is sufficient to restore odor-tracking behavior. These results are the first to demonstrate cellular mechanisms underlying visual-olfactory integration required for odor localization in fruit flies, which may be representative of adaptive multisensory interactions across taxa.
authors.affiliation: Howard Hughes Medical Institute and Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: Sara M
authors.initials: SM
authors.lastname: Wasserman
authors.affiliation: Howard Hughes Medical Institute and Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: Jacob W
authors.initials: JW
authors.lastname: Aptekar
authors.affiliation: Howard Hughes Medical Institute and Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: Patrick
authors.initials: P
authors.lastname: Lu
authors.affiliation: Howard Hughes Medical Institute and Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: Jade
authors.initials: J
authors.lastname: Nguyen
authors.affiliation: Howard Hughes Medical Institute and Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: Austin L
authors.initials: AL
authors.lastname: Wang
authors.affiliation: Howard Hughes Medical Institute and Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: Mehmet F
authors.initials: MF
authors.lastname: Keles
authors.affiliation: Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: Anna
authors.initials: A
authors.lastname: Grygoruk
authors.affiliation: Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA.
authors.forename: David E
authors.initials: DE
authors.lastname: Krantz
authors.affiliation: Medical Research Council Centre for Developmental Biology, King's College London, London SE1 1UL, UK.
authors.forename: Camilla
authors.initials: C
authors.lastname: Larsen
authors.affiliation: Howard Hughes Medical Institute and Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA 90095, USA. Electronic address: frye@ucla.edu.
authors.forename: Mark A
authors.initials: MA
authors.lastname: Frye
mesh_terms: D000818:Animals; D004331:Drosophila melanogaster / Q000502:physiology*; D005260:Female; D018377:Neurotransmitter Agents / Q000378:metabolism; D009812:Odorants; D055696:Olfactory Perception; D011897:Random Allocation; D014796:Visual Perception
chemical_list: D018377:Neurotransmitter Agents