Different classes of input and output neurons reveal new features in microglomeruli of the adult Drosophila mushroom body calyx

Abstract

To investigate how sensory information is processed, transformed, and stored within an olfactory system, we examined the anatomy of the input region, the calyx, of the mushroom bodies of Drosophila melanogaster. These paired structures are important for various behaviors, including olfactory learning and memory. Cells in the input neuropil, the calyx, are organized into an array of microglomeruli each comprising the large synaptic bouton of a projection neuron (PN) from the antennal lobe surrounded by tiny postsynaptic neurites from intrinsic Kenyon cells. Extrinsic neurons of the mushroom body also contribute to the organization of microglomeruli. We employed a combination of genetic reporters to identify single cells in the Drosophila calyx by light microscopy and compared these with cell shapes, synapses, and circuits derived from serial-section electron microscopy. We identified three morphological types of PN boutons, unilobed, clustered, and elongated; defined three ultrastructural types, with clear- or dense-core vesicles and those with a dark cytoplasm having both; reconstructed diverse dendritic specializations of Kenyon cells; and identified Kenyon cell presynaptic sites upon extrinsic neurons. We also report new features of calyx synaptic organization, in particular extensive serial synapses that link calycal extrinsic neurons into a local network, and the numerical proportions of synaptic contacts between calycal neurons. All PN bouton types had more ribbon than nonribbon synapses, dark boutons particularly so, and ribbon synapses were larger and with more postsynaptic elements (2-14) than nonribbon (1-10). The numbers of elements were in direct proportion to presynaptic membrane area. Extrinsic neurons exclusively had ribbon synapses.

What the fly’s nose tells the fly’s brain

“…All axon terminals of antennal lobe projection neurons are found in special structures, called microglomeruli (15), in the mushroom body calyx. Each microglomerulus contains three main components: (i) a single large axon terminal from an antennal lobe projection neuron, (ii) dendritic structures, called claws, from about 10 Kenyon cells, each of which is postsynaptic to the single projection neuron terminal, and (iii) GABAergic terminals from a single anterior paired lateral (APL) neuron that also form synapses on Kenyon cell claws.…”

Mapping chromatic pathways in the Drosophila visual system

“…In a following section, evidence for a presynaptic role in Tm5c is revealed by the presence of clear ~30-nm synaptic vesicles ( Figure 6E). At many synapses in Drosophila, a presynaptic site is revealed by the presence of a bipartite T-bar ribbon, but these are seen neither in all brain regions (for example not in all synapses of the mushroom body calyx, Butcher et al, 2012, nor at all neuromuscular synapses, Atwood et al, 1993), and were also not seen at this depth in the lobula, despite their presence at more distal lobula strata 1 and 2 . It is possible that during DAB incubation they become lost or less visible, and would be seen in unlabeled tissue.…”

Activity-dependent FMRP requirements in development of the neural circuitry of learning and memory

“…The axon continues dorsally and posteriorly to innervate KCs within the MB calyx, with 4-5 microglomeruli (calyx synaptic units; Fig. 1C) (Butcher et al, 2012). Together, these two new transgenic drivers allow labeling and manipulation of two complementary MB-EN classes, thereby permitting investigation of KC input (PN) and output (MVP2) neurons with single-cell resolution.…”