Synaptic organization of the mushroom body calyx in Drosophila melanogaster

Abstract

The calyx neuropil of the mushroom body in adult Drosophila melanogaster contains three major neuronal elements: extrinsic projection neurons, presumed cholinergic, immunoreactive to choline acetyltransferase (ChAT-ir) and vesicular acetylcholine transporter (VAChT-ir) antisera; presumed gamma-aminobutyric acid (GABA)ergic extrinsic neurons with GABA-like immunoreactivity; and local intrinsic Kenyon cells. The projection neurons connecting the calyx with the antennal lobe via the antennocerebral tract are the only source of cholinergic elements in the calyces. Their terminals establish an array of large boutons 2-7 microm in diameter throughout all calycal subdivisions. The GABA-ir extrinsic neurons, different in origin, form a network of fine fibers and boutons codistributed in all calycal regions with the cholinergic terminals and with tiny profiles, mainly Kenyon cell dendrites. We have investigated the synaptic circuits of these three neuron types using preembedding immuno-electron microscopy. All ChAT/VAChT-ir boutons form divergent synapses upon multitudinous surrounding Kenyon cell dendrites. GABA-ir elements also regularly contribute divergent synaptic input onto these dendrites, as well as occasional inputs to boutons of projection neurons. The same synaptic microcircuits involving these three neuron types are repeatedly established in glomeruli in all calycal regions. Each glomerulus comprises a large cholinergic bouton at its core, encircled by tiny vesicle-free Kenyon cell dendrites as well as by a number of GABAergic terminals. A single dendritic profile may thereby receive synaptic input from both cholinergic and GABAergic elements in close vicinity at presynaptic sites with T-bars typical of fly synapses. ChAT-ir boutons regularly have large extensions of the active zones. Thus, Kenyon cells may receive major excitatory input from cholinergic boutons and considerable postsynaptic inhibition from GABAergic terminals, as well as, more rarely, presynaptic inhibitory signaling. The calycal glomeruli of Drosophila are compared with the cerebellar glomeruli of vertebrates. The cholinergic boutons are the largest identified cholinergic synapses in the Drosophila brain and an eligible prospect for studying the genetic regulation of excitatory presynaptic function.

Critical roles of mecamylamine-sensitive mushroom body neurons in insect olfactory learning

“…Second, injection of MEC into the calyces also completely impaired conditioning. Since Kenyon cells receive cholinergic inputs from projection neurons in the calyces (Yasuyama et al, 2002), the neurons affected were no doubt Kenyon cells. We thus suggest that the association occurs in MEC-sensitive…”

“…We evaluated localization of the injected drug by observing the distribution of co-injected (Yasuyama et al, 2002).…”

“…Axons of projection neurons enter the protocerebrum and terminate in the calyces of the mushroom body (MB) and the lateral protocerebrum (LPR) (Yasuyama, Meinertzhagen, & Schümann, 2002;Yasuyama, Meinertzhagen, & Schümann, 2003;Yu, Baird, Tsien, & Davis, 2003). In the calyces, projection neurons make synaptic connections with MB intrinsic neurons, called Kenyon cells (Yasuyama et al, 2002). Axons of Kenyon cells project to the pedunculus and lobes and make synaptic connections with efferent (output) neurons of the MB.…”

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

“…1B), and comprise many thousands of synaptic complexes, called microglomeruli (Yasuyama et al, 2002) that are revealed by phalloidin staining (Fig. 1C and inset).…”

Amyloid-β depresses excitatory cholinergic synaptic transmission in Drosophila

“…After processing in the antennal lobes, olfactory information is relayed by PNs to the mushroom bodies and the protocerebrum. Like other excitatory neurons in the insect central nervous system (CNS), most of these PNs are cholinergic [15] .…”