Visual Input to the Drosophila Central Complex by Developmentally and Functionally Distinct Neuronal Populations

• Published in: Current biology Vol. 27; no. 8; pp. 1098 - 1110
• Main Authors: Omoto, Jaison Jiro, Keleş, Mehmet Fatih, Nguyen, Bao-Chau Minh, Bolanos, Cheyenne, Lovick, Jennifer Kelly, Frye, Mark Arthur, Hartenstein, Volker
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 24.04.2017
• Subjects: central complex; Drosophila; ellipsoid body; insect vision; neural lineage; neuroblast; visual navigation; neural lineage; neuroblast; ellipsoid body; visual navigation; Drosophila; insect vision; central complex
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2017.02.063

The Drosophila central brain consists of stereotyped neural lineages, developmental-structural units of macrocircuitry formed by the sibling neurons of single progenitors called neuroblasts. We demonstrate that the lineage principle guides the connectivity and function of neurons, providing input to the central complex, a collection of neuropil compartments important for visually guided behaviors. One of these compartments is the ellipsoid body (EB), a structure formed largely by the axons of ring (R) neurons, all of which are generated by a single lineage, DALv2. Two further lineages, DALcl1 and DALcl2, produce neurons that connect the anterior optic tubercle, a central brain visual center, with R neurons. Finally, DALcl1/2 receive input from visual projection neurons of the optic lobe medulla, completing a three-legged circuit that we call the anterior visual pathway (AVP). The AVP bears a fundamental resemblance to the sky-compass pathway, a visual navigation circuit described in other insects. Neuroanatomical analysis and two-photon calcium imaging demonstrate that DALcl1 and DALcl2 form two parallel channels, establishing connections with R neurons located in the peripheral and central domains of the EB, respectively. Although neurons of both lineages preferentially respond to bright objects, DALcl1 neurons have small ipsilateral, retinotopically ordered receptive fields, whereas DALcl2 neurons share a large excitatory receptive field in the contralateral hemifield. DALcl2 neurons become inhibited when the object enters the ipsilateral hemifield and display an additional excitation after the object leaves the field of view. Thus, the spatial position of a bright feature, such as a celestial body, may be encoded within this pathway. •We identify a Drosophila brain circuit providing visual input to the central complex•Neuron classes in this circuit are organized based on progenitor origin, or lineage•Two lineages (DALcl1/2) provide parallel input to ellipsoid body ring neurons•DALcl1 and 2 project to discrete domains and transmit different visual information Omoto et al. identify the anterior visual pathway, a circuit in the Drosophila brain consisting of neurons, the structure and function of which are defined by their progenitor origin, or lineage. This circuit is responsible for relaying information from the visual system to the central complex, an important region for visually guided behavior.