Odd‐skipped labels a group of distinct neurons associated with the mushroom body and optic lobe in the adult Drosophila brain

Abstract

Olfactory processing has been intensively studied in Drosophila melanogaster. However, we still know little about the descending neural pathways from the higher order processing centers and how these connect with other neural circuits. Here we describe, in detail, the adult projections patterns that arise from a cluster of 78 neurons, defined by the expression of the Odd-skipped transcription factor. We term these neurons Odd neurons. By using expression of genetically encoded axonal and dendritic markers, we show that a subset of the Odd neurons projects dendrites into the calyx of the mushroom body (MB) and axons into the inferior protocerebrum. We exclude the possibility that the Odd neurons are part of the well-known Kenyon cells whose projections form the MB and conclude that the Odd neurons belong to a previously not described class of extrinsic MB neurons. In addition, three of the Odd neurons project into the lobula plate of the optic lobe, and two of these cells extend axons ipsi- and contralaterally in the brain. Anatomically, these cells do not resemble any previously described lobula plate tangential cells (LPTCs) in Drosophila. We show that the Odd neurons are predominantly cholinergic but also include a small number of γ-aminobutyric acid (GABA)ergic neurons. Finally, we provide evidence that the Odd neurons are a hemilineage, suggesting they are born from a defined set of neuroblasts. Our anatomical analysis hints at the possibility that subgroups of Odd neurons could be involved in olfactory and visual processing.

Olfactory Neuromodulation of Motion Vision Circuitry in Drosophila

“…A lobula plate tangential cell (LPTC) was recently identified anatomically in Drosophila , along with a number of neurons within higher-order olfactory regions of the mushroom bodies, by its shared expression of the Odd-skipped transcription factor [ 9 ]. The tangential dendritic arbor of this LPTC spans the dorsal projection of the lobula plate ( Figure 2 Bi), tightly restricted to layer 2 ( Figures 2 Bii and 2Biii), which is the layer receiving back-to-front directional motion input from the columnar T4T5 terminals [ 23 ].…”

“…The tangential dendritic arbor of this LPTC spans the dorsal projection of the lobula plate ( Figure 2 Bi), tightly restricted to layer 2 ( Figures 2 Bii and 2Biii), which is the layer receiving back-to-front directional motion input from the columnar T4T5 terminals [ 23 ]. The axon projects heterolateral to the cell body and dendrites [ 9 ]. To characterize its motion-coding properties, we expressed a genetically encoded calcium indicator, GCaMP6m [ 25 ], under the Odd-Gal4 driver [ 9 ] and recorded cellular activity under a two-photon excitation imaging system equipped with an LED display [ 26 ] ( Figure 2 A).…”

“…The axon projects heterolateral to the cell body and dendrites [ 9 ]. To characterize its motion-coding properties, we expressed a genetically encoded calcium indicator, GCaMP6m [ 25 ], under the Odd-Gal4 driver [ 9 ] and recorded cellular activity under a two-photon excitation imaging system equipped with an LED display [ 26 ] ( Figure 2 A). Imaging from dendritic regions of interest (ROIs) (see Experimental Procedures ) in response to a narrow vertical bar, we demonstrate that this cell is excited by back-to-front motion across the ipsilateral eye within a 50° receptive field positioned just ipsilateral to the visual midline ( Figure 2 C) and is more excited by progressively wider randomly textured bars ( Figure 2 D).…”

“…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 [ 9, 10 ]. 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 [ 11 ].…”

Motor context coordinates visually guided walking inDrosophila

“…Hx dendrites cover the entire surface of the LP, whereas H2 dendrites avoid the ventral and dorsal region of the LP. In Drosophila, a regressivesensitive cell was previously identified as Hx in a transgenic line for the transcription factor oddskipped (Levy and Larsen, 2013;Wasserman et al, 2015). We electroporated Texas Red at axon terminals of HS cells in a combined transgenic line (VT058487 and odd-Gal4) to compare the labeled cell with the odd-kipped expressing neuron (Fig.…”