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Cell types and coincident synapses in the ellipsoid body of Drosophila

Authors

  • Alfonso Martín-Peña,

    1. Department of Cellular, Molecular and Developmental Neurobiology, Cajal Institute, C.S.I.C., Madrid, Spain
    2. Department of Neurology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, FL, USA
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  • Angel Acebes,

    1. Department of Cellular, Molecular and Developmental Neurobiology, Cajal Institute, C.S.I.C., Madrid, Spain
    2. Center for Biomedical Research of the Canary Islands, Institute of Biomedical Technologies, University of La Laguna, Tenerife, Spain
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  • José-Rodrigo Rodríguez,

    1. Department of Cellular, Molecular and Developmental Neurobiology, Cajal Institute, C.S.I.C., Madrid, Spain
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  • Valerie Chevalier,

    1. Department of Cellular, Molecular and Developmental Neurobiology, Cajal Institute, C.S.I.C., Madrid, Spain
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  • Sergio Casas-Tinto,

    1. Department of Cellular, Molecular and Developmental Neurobiology, Cajal Institute, C.S.I.C., Madrid, Spain
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  • Tilman Triphan,

    1. Biozentrum der Universitaet Wuerzburg, Lehrstuhl für Genetik und Neurobiologie, Wuerzburg, Germany
    2. HHMI Janelia Farm Research Campus, Ashburn, VA, USA
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  • Roland Strauss,

    1. Biozentrum der Universitaet Wuerzburg, Lehrstuhl für Genetik und Neurobiologie, Wuerzburg, Germany
    2. Department of Zoologie III–Neurobiologie, Johannes Gutenberg-Universitaet Mainz, Mainz, Germany
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  • Alberto Ferrús

    Corresponding author
    1. Department of Cellular, Molecular and Developmental Neurobiology, Cajal Institute, C.S.I.C., Madrid, Spain
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Abstract

Cellular ultrastructures for signal integration are unknown in any nervous system. The ellipsoid body (EB) of the Drosophila brain is thought to control locomotion upon integration of various modalities of sensory signals with the animal internal status. However, the expected excitatory and inhibitory input convergence that virtually all brain centres exhibit is not yet described in the EB. Based on the EB expression domains of genetic constructs from the choline acetyl transferase (Cha), glutamic acid decarboxylase (GAD) and tyrosine hydroxylase (TH) genes, we identified a new set of neurons with the characteristic ring-shaped morphology (R neurons) which are presumably cholinergic, in addition to the existing GABA-expressing neurons. The R1 morphological subtype is represented in the Cha- and TH-expressing classes. In addition, using transmission electron microscopy, we identified a novel type of synapse in the EB, which exhibits the precise array of two independent active zones over the same postsynaptic dendritic domain, that we named ‘agora’. This array is compatible with a coincidence detector role, and represents ~8% of all EB synapses in Drosophila. Presumably excitatory R neurons contribute to coincident synapses. Functional silencing of EB neurons by driving genetically tetanus toxin expression either reduces walking speed or alters movement orientation depending on the targeted R neuron subset, thus revealing functional specialisations in the EB for locomotion control.

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