Cell types and coincident synapses in the ellipsoid body of Drosophila

Abstract

Cellular ultrastructures for signal integration are unknown in any nervous system. The ellipsoid body (EB) of the Drosophila brain is thought to control locomotion upon integration of various modalities of sensory signals with the animal internal status. However, the expected excitatory and inhibitory input convergence that virtually all brain centres exhibit is not yet described in the EB. Based on the EB expression domains of genetic constructs from the choline acetyl transferase (Cha), glutamic acid decarboxylase (GAD) and tyrosine hydroxylase (TH) genes, we identified a new set of neurons with the characteristic ring-shaped morphology (R neurons) which are presumably cholinergic, in addition to the existing GABA-expressing neurons. The R1 morphological subtype is represented in the Cha- and TH-expressing classes. In addition, using transmission electron microscopy, we identified a novel type of synapse in the EB, which exhibits the precise array of two independent active zones over the same postsynaptic dendritic domain, that we named 'agora'. This array is compatible with a coincidence detector role, and represents ~8% of all EB synapses in Drosophila. Presumably excitatory R neurons contribute to coincident synapses. Functional silencing of EB neurons by driving genetically tetanus toxin expression either reduces walking speed or alters movement orientation depending on the targeted R neuron subset, thus revealing functional specialisations in the EB for locomotion control.

Ultrastructure of GABA- and Tachykinin-Immunoreactive Neurons in the Lower Division of the Central Body of the Desert Locust

“…Columnar neurons (CL1a-d, CL2) occur as systems of 16 neurons with ramifications in columnar domains of the lower division and projections to the PB, noduli (CL2) or LAL (CL1a, b, d). Similar cell types have been found in other insect species, notably, the monarch butterfly (Heinze et al, 2013) and the fruit fly Drosophila (Hanesch et al, 1989; Martín-Peña et al, 2014; Wolff et al, 2015). In sections largely from the center of the CBL, three types of vesicle could be distinguished in neuronal profiles, small clear vesicles, large dark dense core vesicles and large granular dense core vesicles.…”

“…Dyadic synaptic contacts as found here are the most common synaptic configurations in the nervous system of locusts (Schürmann and Wechsler, 1970; Leitch and Laurent, 1996; Watson and Schürmann, 2002; Träger et al, 2007) and other insect species (e.g., Tolbert and Hildebrand, 1981; Boeckh and Tolbert, 1993; Reischig and Stengl, 2003). In the CBL of Drosophila and the honeybee, in contrast, single (monadic) synapses were reported most frequently (Martín-Peña et al, 2014). These authors also found multiple synapses with two active zones in close proximity and coincident synapses with two presynaptic profiles facing a single postsynaptic profile.…”

The Tiny Drosophila Melanogaster for the Biggest Answers in Huntington’s Disease

“…Moreover, the region-specific gene expression patterns in the developing brain correspond to those in vertebrates. Therefore, the central complex of arthropods and the vertebrate basal ganglia are homologous brain structures that both share topography and embryological derivation, as well as functionality and gene expression [66,67]. The central complex structure is highly conserved across the insect species [68].…”

“…The perturbation of dopaminergic pathway activity, or its modulatory output interferes with the corresponding behavioral actions, common in age-related degeneration of the dopaminergic clusters, and typical of HD. As in the neostriatum, the central complex displays a strong GABA neurotransmitter and receptor expression, at least in the ellipsoid body neuropil [66,67]. …”

Building a functional connectome of the Drosophila central complex

“…First, the two ring neuron types we tested (GB-Eo, L-Ei) target the wedge columnar neurons (E-PG, Figure S5Ai), as has been suggested previously (Martín-Peña et al, 2014;Kahsai et al, 2012;Hanesch et al, 1989). Note that the ring neurons presented here are non-canonical : they do not innervate the bulb but either the LAL or the Gall.…”