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

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.

SUBMITTER: Omoto JJ

PROVIDER: S-EPMC6278638 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Neuronal Constituents and Putative Interactions Within the <i>Drosophila</i> Ellipsoid Body Neuropil.

Omoto Jaison Jiro JJ Nguyen Bao-Chau Minh BM Kandimalla Pratyush P Lovick Jennifer Kelly JK Donlea Jeffrey Michael JM Hartenstein Volker V

Frontiers in neural circuits 20181127

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 <i>Drosophila</i> CX. The neuropil volume of the EB, along with its prominent input compartment, called the bulb, is subdivided into precisely tessellated domain ...[more]

PMID: 30546298

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Project description:BackgroundThe mushroom bodies (MBs) of Drosophila are required for complex behaviors and consist of three types of neurons, gamma, alpha'/beta' and alpha/beta. Previously, roles for transcription factors in MB neuronal differentiation have only been described for a subset of MB neurons. We are investigating the roles of unfulfilled (unf; HR51, CG16801) in MB development. unf encodes a nuclear receptor that is orthologous to the nuclear receptors fasciculation of axons defective 1 (FAX-1) of the nematode and photoreceptor specific nuclear receptor (PNR) of mammals. Based on our previous observations that unf transcripts accumulate in MB neurons at all developmental stages and the presence of axon pathfinding defects in fax-1 mutants, we hypothesized that unf regulates MB axon growth and pathfinding.ResultsWe show that unf mutants exhibit a range of highly penetrant axon stalling phenotypes affecting all neurons of the larval and adult MBs. Phenotypic analysis of unfX1 mutants revealed that alpha'/beta' and alpha/beta neurons initially project axons but stall prior to the formation of medial or dorsal MB lobes. unfZ0001 mutants form medial lobes, although these axons fail to branch, which results in a failure to form the alpha or alpha' dorsal lobes. In either mutant background, gamma neurons fail to develop larval-specific dorsal projections. These mutant gamma neurons undergo normal pruning, but fail to re-extend axons medially during pupal development. unfRNAi animals displayed phenotypes similar to those seen in unfZ0001 mutants. Unique asymmetrical phenotypes were observed in unfX1/unfZ0001 compound heterozygotes. Expression of UAS-unf transgenes in MB neurons rescues the larval and adult unf mutant phenotypes.ConclusionsThese data support the hypothesis that unf plays a common role in the development of all types of MB neurons. Our data indicate that unf is necessary for MB axon extension and branching and that the formation of dorsal collaterals is more sensitive to the loss of unf function than medial projections. The asymmetrical phenotypes observed in compound heterozygotes support the hypothesis that the earliest MB axons may serve as pioneers for the later-born MB neurons, providing evidence for pioneer MB axon guidance in post-embryonic development.

Project description:The ellipsoid body (EB) is a major structure of the central complex of the Drosophila melanogaster brain. Twenty-two subtypes of EB ring neurons have been identified based on anatomic and morphologic characteristics by light-level microscopy and EM connectomics. A few studies have associated ring neurons with the regulation of sleep homeostasis and structure. However, cell type-specific and population interactions in the regulation of sleep remain unclear. Using an unbiased thermogenetic screen of EB drivers using female flies, we found the following: (1) multiple ring neurons are involved in the modulation of amount of sleep and structure in a synergistic manner; (2) analysis of data for ΔP(doze)/ΔP(wake) using a mixed Gaussian model detected 5 clusters of GAL4 drivers which had similar effects on sleep pressure and/or depth: lines driving arousal contained R4m neurons, whereas lines that increased sleep pressure had R3m cells; (3) a GLM analysis correlating ring cell subtype and activity-dependent changes in sleep parameters across all lines identified several cell types significantly associated with specific sleep effects: R3p was daytime sleep-promoting, and R4m was nighttime wake-promoting; and (4) R3d cells present in 5HT7-GAL4 and in GAL4 lines, which exclusively affect sleep structure, were found to contribute to fragmentation of sleep during both day and night. Thus, multiple subtypes of ring neurons distinctively control sleep amount and/or structure. The unique highly interconnected structure of the EB suggests a local-network model worth future investigation; understanding EB subtype interactions may provide insight how sleep circuits in general are structured.SIGNIFICANCE STATEMENT How multiple brain regions, with many cell types, can coherently regulate sleep remains unclear, but identification of cell type-specific roles can generate opportunities for understanding the principles of integration and cooperation. The ellipsoid body (EB) of the fly brain exhibits a high level of connectivity and functional heterogeneity yet is able to tune multiple behaviors in real-time, including sleep. Leveraging the powerful genetic tools available in Drosophila and recent progress in the characterization of the morphology and connectivity of EB ring neurons, we identify several EB subtypes specifically associated with distinct aspects of sleep. Our findings will aid in revealing the rules of coding and integration in the brain.

Project description:The paired box gene Pox neuro (Poxn) is expressed in two bilaterally symmetric neuronal clusters of the developing adult Drosophila brain, a protocerebral dorsal cluster (DC) and a deutocerebral ventral cluster (VC). We show that all cells that express Poxn in the developing brain are postmitotic neurons. During embryogenesis, the DC and VC consist of only 20 and 12 neurons that express Poxn, designated embryonic Poxn-neurons. The number of Poxn-neurons increases only during the third larval instar, when the DC and VC increase dramatically to about 242 and 109 Poxn-neurons, respectively, virtually all of which survive to the adult stage, while no new Poxn-neurons are added during metamorphosis. Although the vast majority of Poxn-neurons express Poxn only during third instar, about half of them are born by the end of embryogenesis, as demonstrated by the absence of BrdU incorporation during larval stages. At late third instar, embryonic Poxn-neurons, which begin to express Poxn during embryogenesis, can be easily distinguished from embryonic-born and larval-born Poxn-neurons, which begin to express Poxn only during third instar, (i) by the absence of Pros, (ii) their overt differentiation of axons and neurites, and (iii) the strikingly larger diameter of their cell bodies still apparent in the adult brain. The embryonic Poxn-neurons are primary neurons that lay out the pioneering tracts for the secondary Poxn-neurons, which differentiate projections and axons that follow those of the primary neurons during metamorphosis. The DC and the VC participate only in two neuropils of the adult brain. The DC forms most, if not all, of the neurons that connect the bulb (lateral triangle) with the ellipsoid body, a prominent neuropil of the central complex, while the VC forms most of the ventral projection neurons of the antennal lobe, which connect it ipsilaterally to the lateral horn, bypassing the mushroom bodies. In addition, Poxn-neurons of the VC are ventral local interneurons of the antennal lobe. In the absence of Poxn protein in the developing brain, embryonic Poxn-neurons stall their projections and cannot find their proper target neuropils, the bulb and ellipsoid body in the case of the DC, or the antennal lobe and lateral horn in the case of the VC, whereby the absence of the ellipsoid body neuropil is particularly striking. Poxn is thus crucial for pathfinding both in the DC and VC. Additional implications of our results are discussed.

Dataset Information

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

Publications

Neuronal Constituents and Putative Interactions Within the <i>Drosophila</i> Ellipsoid Body Neuropil.

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