Neuronal Constituents and Putative Interactions Within the Drosophila Ellipsoid Body Neuropil.

Jaison Jiro Omoto,Jeffrey Michael Donlea,Jennifer Kelly Lovick,Pratyush Kandimalla,Volker Hartenstein,Bao-Chau Minh Nguyen

doi:10.3389/fncir.2018.00103

Jaison Jiro Omoto, Jeffrey Michael Donlea + Show 4 more

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https://doi.org/10.3389/fncir.2018.00103

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Abstract

The central complex (CX) is a midline-situated collection of neuropil compartments in the arthropod central brain, implicated in higher-order processes such as goal-directed navigation. Here, we provide a systematic genetic-neuroanatomical analysis of the ellipsoid body (EB), a compartment which represents a major afferent portal of the Drosophila CX. The neuropil volume of the EB, along with its prominent input compartment, called the bulb, is subdivided into precisely tessellated domains, distinguishable based on intensity of the global marker DN-cadherin. EB tangential elements (so-called ring neurons), most of which are derived from the DALv2 neuroblast lineage, predominantly interconnect the bulb and EB domains in a topographically organized fashion. Using the DN-cadherin domains as a framework, we first characterized this connectivity by Gal4 driver lines expressed in different DALv2 ring neuron (R-neuron) subclasses. We identified 11 subclasses, 6 of which correspond to previously described projection patterns, and 5 novel patterns. These subclasses both spatially (based on EB innervation pattern) and numerically (cell counts) summate to the total EB volume and R-neuron cell number, suggesting that our compilation of R-neuron subclasses approaches completion. EB columnar elements, as well as non-DALv2 derived extrinsic ring neurons (ExR-neurons), were also incorporated into this anatomical framework. Finally, we addressed the connectivity between R-neurons and their targets, using the anterograde trans-synaptic labeling method, trans-Tango. This study demonstrates putative interactions of R-neuron subclasses and reveals general principles of information flow within the EB network. Our work will facilitate the generation and testing of hypotheses regarding circuit interactions within the EB and the rest of the CX.

Highlights

The central complex (CX) is an evolutionarily conserved, higher-order neuropil in the arthropod brain thought to integrate sensory and motor information to coordinate and maintain locomotor behavior, enabling appropriate navigation
R5 In a previous paper (Omoto et al, 2017) we described an additional subclass of outer ring neurons called R5, labeled by 58H05-Gal4, which targets the small, anterior ellipsoid body (EB) domain (EBa; Figure 3C and Supplementary Movies 19, 20; 14 ± 1 neurons per brain hemisphere (PBH))
In accordance with the notion that R3d and R4d are postsynaptic partners of R2, we find trans-Tango labeling in a posterior-lateral part of BUs (Figure 10B5), shown above to be dendritically innervated by R4d, FIGURE 10 | Putative postsynaptic partners of R-neurons revealed by trans-Tango. (A–D) Confocal z-projections of Gal4 drivers that label distinct R-neuron subclasses in conjunction with trans-Tango mediated labeling of postsynaptic neurons

Summary

Introduction

The central complex (CX) is an evolutionarily conserved, higher-order neuropil in the arthropod brain thought to integrate sensory and motor information to coordinate and maintain locomotor behavior, enabling appropriate navigation. Electrical stimulation of CX neurons in the freely walking cockroach has yielded direct evidence linking CX activity to downstream locomotor output (Martin et al, 2015). In other insects, such as locust, cricket, monarch butterfly, and dung beetle, neurons in the CX are tuned to celestial visual cues such as the sun or pattern of polarized skylight. These cues provide the stable environmental signals required to accurately derive relative heading information for short or long range navigations (Heinze and Homberg, 2007; Heinze and Reppert, 2011; el Jundi et al, 2014, 2015)

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