Presynapses in Kenyon Cell Dendrites in the Mushroom Body Calyx of Drosophila

Abstract

Plastic changes at the presynaptic sites of the mushroom body (MB) principal neurons called Kenyon cells (KCs) are considered to represent a neuronal substrate underlying olfactory learning and memory. It is generally believed that presynaptic and postsynaptic sites of KCs are spatially segregated. In the MB calyx, KCs receive olfactory input from projection neurons (PNs) on their dendrites. Their presynaptic sites, however, are thought to be restricted to the axonal projections within the MB lobes. Here, we show that KCs also form presynapses along their calycal dendrites, by using novel transgenic tools for visualizing presynaptic active zones and postsynaptic densities. At these presynapses, vesicle release following stimulation could be observed. They reside at a distance from the PN input into the KC dendrites, suggesting that regions of presynaptic and postsynaptic differentiation are segregated along individual KC dendrites. KC presynapses are present in ␥-type KCs that support short-and long-term memory in adult flies and larvae. They can also be observed in ␣/␤-type KCs, which are involved in memory retrieval, but not in ␣Ј/␤Ј-type KCs, which are implicated in memory acquisition and consolidation. We hypothesize that, as in mammals, recurrent activity loops might operate for memory retrieval in the fly olfactory system. The newly identified KC-derived presynapses in the calyx are, inter alia, candidate sites for the formation of memory traces during olfactory learning.

A Central Neural Pathway Controlling Odor Tracking inDrosophila

“…We also demonstrate reconstitution of GFP between Kenyon cells and the Odd neurons. Presynaptic densities have been observed in the Kenyon cell dendrites (Christiansen et al, 2011), and, while the extent of labeling between Kenyon cells and the Odd neurons is less extensive than that seen between the Odd neurons and PNs, it suggests that the Odd neurons are connected with Kenyon cells. In that case, these connections must be dendro-dendritic synapses, and, as such, it is not possible to infer directionality from the GRASP studies.…”

“…For the Mosaic Analysis with a Repressible Cell Marker (MARCM) clones, we used, in addition to the Odd-Gal4 line, FRT 19A,and FRT19A,, and Dynein mutant (Zheng et al, 2008). GFP reconstruction across synaptic partners (GRASP) was performed using, in combination with the Odd-Gal4 driver, GH146-LexA-GAD (Sudhakaran et al, 2012), MB247-LexA-VP16 (Burke et al, 2012), UAS-CD4::spGFP1-10, and LexAop-CD4::spGFP11 (Kreher et al, 2008). For functional imaging UAS-GCaMP6(fast) (Bloomington Stock Center; Akerboom et al, 2012) was driven using the Odd-Gal4 line.…”

Mapping chromatic pathways in the Drosophila visual system

“…To understand how color information is processed in the deep visual centers, we set out to identify the synaptic targets of these chromatic Tm neurons. First, we used the ort C1a -LexAVP16 driver to express an active-zone marker, Brp D3 ::mCherry, in all four types of Tm neurons, to mark their presynaptic sites (Christiansen et al, 2011;Karuppudurai et al, 2014;Ting et al, 2014;Melnattur et al, 2014). We found that the presynaptic sites of these neurons were localized to the axon terminals in the deep lobula strata, Lo4-6 (Fischbach and Dittrich, 1989; Figure 1B1), as well as their dendrites in the medulla (stratum M8; Figure 1B).…”

Requirement of the combination of mushroom body γ lobe and α/β lobes for the retrieval of both aversive and appetitive early memories in Drosophila

“…It is possible that there may be some communication between g lobe neurons and a/b lobe neurons before or during memory retrieval. This communication can be mediated by MB intrinsic neurons and extrinsic neurons (Krashes et al 2007;Lee et al 2011;Qin et al 2012), or achieved by direct interaction (Christiansen et al 2011).…”