Visual Input to the Drosophila Central Complex by Developmentally and Functionally Distinct Neuronal Populations

Omoto, Jaison J.; Keleş, Mehmet F.; Nguyen, Bao-Chau Minh; Bolanos, Cheyenne; Lovick, Jennifer K.; Frye, Mark A.; Hartenstein, Volker

doi:10.1016/j.cub.2017.02.063

Cited by 147 publications

(355 citation statements)

References 53 publications

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“…Internally, however, the bulb differed in the organization of GABA immunolabeling. In many species the bulb was a uniform entity, in others it was subdivided into distinct areas (Figures d, b, d,g, and d) indicating distinct subtypes of TL/R neurons (Müller et al, ; Omoto et al, ). An internal organization into microglomeruli up to a size of small somata was found in most butterfly species.…”

Section: Discussionmentioning

confidence: 99%

GABA immunostaining in the central complex of dicondylian insects

Homberg

Humberg

Seyfarth

et al. 2018

J of Comparative Neurology

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The central complex is a group of midline-crossing neuropils in the insect brain involved in head direction coding, sky compass navigation, and spatial visual memory. To compare the neuroarchitecture and neurochemistry of the central complex in insects that differ in locomotion, ways of orientation, time of activity (diurnal, nocturnal), and evolutionary history, we studied the distribution of γ-aminobutyric acid (GABA) immunostaining in the central complex of 29 species, ranging from Zygentoma to Diptera. In all species, the lower division of the central body was densely innervated by GABA-immunoreactive tangential neurons. These neurons had additional arborizations in the bulb, a distinct region of synaptic complexes in the lateral complex, and somata in a cell cluster mediodorsally to the antennal lobe. Differences in the appearance of GABA immunostaining in the lower division of the central body corresponded to differences in neuropil architecture, such as transformation of the lower division into a toroid in certain Diptera and Heteroptera. In nearly all species two additional systems of tangential neuron of the upper division of the central body were GABA-immunoreactive. One of these systems diffusely invaded a superior layer, while the second system showed fan-like projections in an inferior layer. Sparse immunostaining in the protocerebral bridge was detected in cockroaches, a cricket, and two hemipteran species. The data show that three systems of GABA-immunoreactive tangential neurons of the central body are highly conserved and suggest that the layered organization of the upper division of the central body is, likewise, largely maintained from basal to advanced species.

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Section: Discussionmentioning

confidence: 99%

GABA immunostaining in the central complex of dicondylian insects

Homberg

Humberg

Seyfarth

et al. 2018

J of Comparative Neurology

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“…In previous studies, DNcad has been used to define discrete compartments in the neuropile of the central brain. In particular, the so called “structured neuropil”, including the central complex, mushroom body, or antennal lobe exhibits modular subdivisions that are revealed by DNcad, or other markers that primarily highlight synaptic density (Pereanu et al, 2010; Ito et al, 2014; Omoto et al, 2017). The simultaneous labeling of all medulla layers by global marking techniques, rather than specific genetic markers that can only visualize one type of neuron/layer at a time, will be useful for future studies relying on the anatomical mapping of individual neurons, or classes of neurons.…”

Section: Discussionmentioning

confidence: 99%

Spatio-temporal pattern of neuronal differentiation in the Drosophila visual system: A user’s guide to the dynamic morphology of the developing optic lobe

Ngo¹,

Andrade²,

Hartenstein

2017

Developmental Biology

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Visual information processing in animals with large image forming eyes is carried out in highly structured retinotopically ordered neuropils. Visual neuropils in Drosophila form the optic lobe, which consists of four serially arranged major subdivisions; the lamina, medulla, lobula and lobula plate; the latter three of these are further subdivided into multiple layers. The visual neuropils are formed by more than 100 different cell types, distributed and interconnected in an invariant highly regular pattern. This pattern relies on a protracted sequence of developmental steps, whereby different cell types are born at specific time points and nerve connections are formed in a tightly controlled sequence that has to be coordinated among the different visual neuropils. The developing fly visual system has become a highly regarded and widely studied paradigm to investigate the genetic mechanisms that control the formation of neural circuits. However, these studies are often made difficult by the complex and shifting patterns in which different types of neurons and their connections are distributed throughout development. In the present paper we have reconstructed the three-dimensional architecture of the Drosophila optic lobe from the early larva to the adult. Based on specific markers, we were able to distinguish the populations of progenitors of the four optic neuropils and map the neurons and their connections. Our paper presents sets of annotated confocal z-projections and animated 3D digital models of these structures for representative stages. The data reveal the temporally coordinated growth of the optic neuropils, and clarify how the position and orientation of the neuropils and interconnecting tracts (inner and outer optic chiasm) changes over time. Finally, we have analyzed the emergence of the discrete layers of the medulla and lobula complex using the same markers (DN-cadherin, Brp) employed to systematically explore the structure and development of the central brain neuropil. Our work will facilitate experimental studies of the molecular mechanisms regulating neuronal fate and connectivity in the fly visual system, which bears many fundamental similarities with the retina of vertebrates.

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“…In a recent study we had shown that the neural circuit providing visual input to the central complex, the anterior visual pathway (AVP), is formed by three lineages, DALv2, DALcl1, and DALcl2 (Omoto et al, ). Larvally‐born (secondary) neurons of DALv2 are confined to the ellipsoid body (EB) and its input compartment, the bulb (BU; Larsen et al, ; Spindler & Hartenstein, ; Wong et al, ; Figure ).…”

Section: Introductionmentioning

confidence: 99%

“… Anterior visual pathway of the Drosophila brain. Schematic frontal view of brain hemisphere depicting the neuronal elements forming the anterior visual pathway, as described in Omoto et al (). Medullo‐tubercular (MeTu) neurons project via the anterior optic tract to the lateral and intermediate domain of the anterior optic tubercle; AOTU).…”

Section: Introductionmentioning

confidence: 99%

“…Input to the BU originates in the anterior optic tubercle (AOTU), which in turn is a recipient of visual interneurons from the medulla. Two hemilineages (sets of neurons derived from the unequal division of the ganglion mother cells; Truman, Moats, Altman, Marin, & Williams, ), DALcl1d and DALcl2d (Omoto et al, ), form a topographically ordered projection from AOTU to BU that respects the boundaries set by the subclasses of DALv2 ring neurons. DALcl1 and DALcl2 are two neighboring lineages with cell bodies in the dorso‐anterior cortex.…”

Section: Introductionmentioning

confidence: 99%

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Development of the anterior visual input pathway to the Drosophila central complex

Lovick

Omoto

Ngo

et al. 2017

J of Comparative Neurology

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The anterior visual pathway (AVP) conducts visual information from the medulla of the optic lobe via the anterior optic tubercle (AOTU) and bulb (BU) to the ellipsoid body (EB) of the central complex. The anatomically defined neuron classes connecting the AOTU, BU, and EB represent discrete lineages, genetically and developmentally specified sets of cells derived from common progenitors (Omoto et al., 2017). In this paper, we have analyzed the formation of the AVP from early larval to adult stages. The immature fiber tracts of the AVP, formed by secondary neurons of lineages DALcl1/2 and DALv2, assemble into structurally distinct primordia of the AOTU, BU, and EB within the late larval brain. During the early pupal period (P6-P48) these primordia grow in size and differentiate into the definitive subcompartments of the AOTU, BU, and EB. The primordium of the EB has a complex composition. DALv2 neurons form the anterior EB primordium, which starts out as a bilateral structure, then crosses the midline between P6 and P12, and subsequently bends to adopt the ring shape of the mature EB. Columnar neurons of the central complex, generated by the type II lineages DM1-4, form the posterior EB primordium. Starting out as an integral part of the fan-shaped body (FB) primordium, the posterior EB primordium moves forward and merges with the anterior EB primordium. We document the extension of neuropil glia around the nascent EB and BU, and analyze the relationship of primary and secondary neurons of the AVP lineages.

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Visual Input to the Drosophila Central Complex by Developmentally and Functionally Distinct Neuronal Populations

Cited by 147 publications

References 53 publications

GABA immunostaining in the central complex of dicondylian insects

GABA immunostaining in the central complex of dicondylian insects

Spatio-temporal pattern of neuronal differentiation in the Drosophila visual system: A user’s guide to the dynamic morphology of the developing optic lobe

Development of the anterior visual input pathway to the Drosophila central complex

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