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. 2020 Dec 14;9:e62576. doi: 10.7554/eLife.62576

Figure 2. Anatomy of the adult Drosophila MB.

Diagram of structure and information flow in the MB. (A) An image of the brain showing subregions of the MB (see panel B for more detail) and examples of the sensory pathways that provide information to the KCs. Projection neurons (PNs) from the 51 olfactory glomeruli of the antennal lobe (AL) extend axons to the calyx (CA) of the MB and the lateral horn (LH). A total of 126 PNs, using a threshold of 25 synapses, innervate the CA and two innervate the lACA. Six olfactory PNs from the DL3 glomerulus are shown (white). Also shown is a visual projection neuron, aMe12 (red) that conveys information from the optic lobe (OL) to the ventral accessory calyx (vACA) and a thermosensory projection neuron (green) that conveys cold temperature information from arista sensory neurons in glomerulus VP3 to the lACA; the positions of the accessory calyces are shown in (B). See Figure 1—video 1 for additional details. (B) Subregions within the MB. The γ lobe, CA, and pedunculus are displayed separately from other lobes; their normal positions are as shown in panel A. Color-coding is as in panel A. (C) The MB output neuron (MBON14) whose dendrites fill the α3 compartment at the tip of the vertical lobe is shown along with the dopaminergic neuron (PPL106), whose axonal terminals lie in the same compartment. See Figure 1—video 2 for more detailed examples of the structure of a compartment. (D) A schematic representation of the key cellular components and information flow during processing of sensory inputs to the MB. Olfactory receptor neurons (ORNs) expressing the same odorant receptor converge onto a single glomerulus in the AL. A small number (generally 3 – 4) of PNs from each of the 51 olfactory glomeruli innervate the MB, where they synapse on the dendrites of the ~2000 Kenyon cells (KCs) in a globular structure, the CA. Each KC exhibits, on average, six dendritic ‘claws’, and each claw is innervated by a single PN. The axons of the KCs project in parallel anteriorly through the pedunculus (ped) to the lobes, where KCs synapse onto the dendrites of MB output neurons (MBONs). KCs can be categorized into three major classes α/β, α′/β′, and γ, based on their projection patterns in the lobes (Crittenden et al., 1998). The β, β′, and γ lobes constitute the medial lobes (also known as horizontal lobes), while the α and α′ lobes constitute the vertical lobes. These lobes are separately wrapped by ensheathing glia (Awasaki et al., 2008). The α/β and α′/β′ neurons bifurcate at the anterior end of the ped (pedc) and project to both the medial and vertical lobes (Lee et al., 1999). The γ neurons project only to the medial lobe. Dendrites of MBONs and terminals of modulatory dopaminergic neurons (DANs) intersect the longitudinal axis of the KC axon bundle, forming 15 subdomains or compartments, five each in the α/β, α′/β′, and γ lobes (numbered α1, α2, and α3 for the compartments in the α lobe from proximal to distal and similarly for the other lobes; Aso et al., 2014a; Tanaka et al., 2008). Additionally, one MBON and one DAN innervate the core of the distal pedunculus (pedc) intersecting the α/β KCs. In the current work, we further classified KCs into 14 types, 10 main types and four unusual embryonic born KCs, named KCγs1-s4 (see Figure 3); the main KC types have their dendrites in the main calyx, with the following exceptions: The dendrites of γd KCs form the ventral accessory calyx (vACA; Aso et al., 2009; Butcher et al., 2012); those of the α/βp KCs form the dorsal accessory calyx (dACA; Lin et al., 2007; Tanaka et al., 2008); and the dendrites of a subset of α′/β′ cells form the lateral accessory calyx (lACA) (Marin et al., 2020; Yagi et al., 2016). These accessory calyces receive non-olfactory input (Tanaka et al., 2008). Different KCs occupy distinct layers in the lobes as indicated (p: posterior; c: core; s: surface; a: anterior; m: middle, main and d: dorsal). Some MB extrinsic neurons extend processes only to a specific layer within a compartment. (E) Individual compartments serve as parallel units of memory formation (see Aso and Rubin, 2016). Reward or punishment is conveyed by dopaminergic neurons, and the coincidence of dopamine release with activity of a KC modifies the strength of that KC’s synapses onto the MBONs in that compartment. The circuit structure by which those MBONs combine their outputs to influence behavior and provide feedback to dopaminergic neurons are investigated in this paper.

Figure 2.

Figure 2—figure supplement 1. The extent of the hemibrain volume and key to brain area nomenclature.

Figure 2—figure supplement 1.

(A) The portion of the central brain (light blue) that was imaged and reconstructed to generate the hemibrain volume (Scheffer et al., 2020) is superimposed on a frontal view of a grayscale representation of the entire Drosophila brain (JRC 2018 unisex template; Bogovic et al., 2018). The mushroom body (MB) is shown in purple. The midline is indicated by the dotted black line. The brain areas LO, ME, and SEZ, which largely lie outside the hemibrain, are labeled. (B) The same structures viewed from the posterior side of the brain. (C, D) Labeled brain regions in the area indicated by the yellow boxes in panels A and B, respectively. The table shows the abbreviations and full names for brain regions discussed in this paper. See Scheffer et al., 2020 for details.