Genetic analysis of the Drosophila ellipsoid body neuropil: Organization and development of the central complex

Renn, Susan C. P.; Armstrong, J. D.; Yang, Mingyao; Wang, Zongsheng; Xu, An; Kaiser, Kim; Taghert, Paul H.

doi:10.1002/(sici)1097-4695(19991105)41:2<189::aid-neu3>3.3.co;2-h

Cited by 81 publications

(140 citation statements)

References 23 publications

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“…The ellipsoid body contains ten types of small-field neurons that connect it to other central complex substructures (for example, the fan-shaped body) 13 . It also contains at least six types of large-field (R) neurons that arborize as a ring, mainly in the anterior part 13,28 . Genetic mosaic flip-out analyses and immunolabeling indicated that the dNR2-positive neurons are the large-field, R4m subtype (H.-H. Lin, and A.-S.C., unpublished data).…”

Section: Resultsmentioning

confidence: 99%

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

et al. 2007

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In humans and many other animals, memory consolidation occurs through multiple temporal phases and usually involves more than one neuroanatomical brain system. Genetic dissection of Pavlovian olfactory learning in Drosophila melanogaster has revealed multiple memory phases, but the predominant view holds that all memory phases occur in mushroom body neurons. Here, we demonstrate an acute requirement for NMDA receptors (NMDARs) outside of the mushroom body during long-term memory (LTM) consolidation. Targeted dsRNA-mediated silencing of Nmdar1 and Nmdar2 (also known as dNR1 or dNR2, respectively) in cholinergic R4m-subtype large-field neurons of the ellipsoid body specifically disrupted LTM consolidation, but not retrieval. Similar silencing of functional NMDARs in the mushroom body disrupted an earlier memory phase, leaving LTM intact. Our results clearly establish an anatomical site outside of the mushroom body involved with LTM consolidation, thus revealing both a distributed brain system subserving olfactory memory formation and the existence of a system-level memory consolidation in Drosophila.Pavlovian olfactory learning in Drosophila creates an elemental associative memory in a simple, accessible insect brain. This form of behavioral plasticity requires the normal function of NMDARs 1 , as is the case in other invertebrate and vertebrate species 2,3 . Memory formation in flies thereafter proceeds through several temporal phases and involves multiple biochemical cascades, which is again similar to findings from other animal models 4-6 . In particular, spaced training produces stronger, longer-lasting memory than massed training, which is a common property of memory formation 7,8 . Contrary to the fact that memory storage involves multiple anatomical regions in other animal models 9 , olfactory memory has been proposed to be stored predominantly in the mushroom body neurons 5,10 .The mushroom body is a prominent neuropillar structure in the insect central brain. Intrinsic mushroom body cells send neurites ventrally into the calyx, a region of dendritic arborization that is innervated by efferents from several different regions, including projection neurons from the antennal lobes 11 . Mushroom body axons project rostrally as a densely packed and stalk-like structure called the pedunculus to the anterior face of the brain, where they split and give rise to the dorsally projecting a and a¢ lobes and the medially projecting b, b¢ and g lobes 12 . Output neurons from the mushroom body project to many parts of the central brain. Another prominent neuropil is the central complex, which consists of four substructures, the ellipsoid body, the fan-shaped body, the nodulii and the protocerebral bridge. The central complex lies in the central brain between the pedunculi of the mushroom body and is bounded laterally by the two antennoglomerular tracts, dorsally by the pars intercerebralis, ventrally by the esophagus and the great commissure and frontally by the median bundle and the b-lobes of the mushroom bodies fronta...

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Section: Resultsmentioning

confidence: 99%

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

et al. 2007

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“…The EB is organized in a concentric pattern of glomeruli with major contributions from the projections of large-field ring or R neurons (Fig. 4C) (40,41). A subgroup of these, the R2/R4 EB neurons, mediate both ethanolinduced hyperactivity (33) and ethanol tolerance (42,43).…”

Section: Different Subsets Of Dopamine Neurons Drive Competing Behavimentioning

confidence: 99%

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Azanchi

Kaun

Heberlein

2013

Proc. Natl. Acad. Sci. U.S.A.

101

100

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The neural circuits that mediate behavioral choice evaluate and integrate information from the environment with internal demands and then initiate a behavioral response. Even circuits that support simple decisions remain poorly understood. In Drosophila melanogaster, oviposition on a substrate containing ethanol enhances fitness; however, little is known about the neural mechanisms mediating this important choice behavior. Here, we characterize the neural modulation of this simple choice and show that distinct subsets of dopaminergic neurons compete to either enhance or inhibit egg-laying preference for ethanol-containing food. Moreover, activity in α′β′ neurons of the mushroom body and a subset of ellipsoid body ring neurons (R2) is required for this choice. We propose a model where competing dopaminergic systems modulate oviposition preference to adjust to changes in natural oviposition substrates.I n nature, rotting fruit is the social hub for the fruit fly Drosophila melanogaster. Flies use fermenting fruit as a food source (1) and a site for oviposition (2). The choice of a suitable oviposition substrate is an ecologically important decision with a direct impact on species fitness. However, other than having a clear preference for fermenting fruit, how females choose oviposition sites in nature is largely unknown.One of the main metabolites of fermentation is ethanol, which is present in ripe fleshy fruits (3). Although ethanol concentrations in the fruit are rather low [≤5% (vol/vol)] (4), plumes containing ethanol vapor can act as long-distance signals to attract flies to rotting fruit (3, 5). When given the choice, female flies prefer to lay their eggs on media containing low concentrations of ethanol (up to 5%) (6), which leads to enhanced fitness of the developing larva and the adult fly.D. melanogaster's resistance to ethanol toxicity may have evolved to allow inhabitation of ethanol-containing environments (7). For example, adult flies allowed to mate on ethanolcontaining media improve mating success and fecundity (8). Although rearing larvae on food containing relatively high ethanol concentrations delays development and decreases survival (9-11), larvae reared on low concentrations of ethanol develop into heavier adults (7,12). This weight increase may be a result of D. melanogaster larvae metabolizing ethanol and using it as a food source (12). Ingestion of ethanol during the larval stage has additional benefits, such as protection from natural parasites such as endoparasitoid wasps (13).Studies on the neural circuits underlying the oviposition program and choice of oviposition substrates have been initiated only recently in D. melanogaster (14, 15). Ethanol is a particularly intriguing stimulus for oviposition preference, because it has, depending on concentration, both beneficial and detrimental effects on developing larvae. In flies, the function of dopaminergic neurons has been implicated in responses to both rewarding and aversive stimuli (16-19), making it a candidate neuromodulator to signa...

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“…8 E). The ellipsoid body precursor, a flat neuropilic structure consisting of dorsal fibers, elongates downward during metamorphosis to form the final adult ring shape (Renn et al, 1999;Boquet et al, 2000). Thus, we believe the phenotype observed in vav mutants is most likely due to ellipsoid body neurons failing to achieve complete growth.…”

Section: Vav Is Required For the Correct Growth Of Axons Forming The mentioning

confidence: 99%

The Guanine Exchange FactorvavControls Axon Growth and Guidance duringDrosophilaDevelopment

Malartre

Ayaz²,

Amador³

et al. 2010

J. Neurosci.

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The Vav proteins are guanine exchange factors (GEFs) that trigger the activation of the Rho GTPases in general and the Rac family in particular. While the role of the mammalian vav genes has been extensively studied in the hematopoietic system and the immune response, there is little information regarding the role of vav outside of these systems. Here, we report that the single Drosophila vav homolog is ubiquitously expressed during development, although it is enriched along the embryonic ventral midline and in the larval eye discs and brain. We have analyzed the role that vav plays during development by generating Drosophila null mutant alleles. Our results indicate that vav is required during embryogenesis to prevent longitudinal axons from crossing the midline. Later on, during larval development, vav is required within the axons to regulate photoreceptor axon targeting to the optic lobe. Finally, we demonstrate that adult vav mutant escapers, which exhibit coordination problems, display axon growth defects in the ellipsoid body, a brain area associated with locomotion control. In addition, we show that vav interacts with other GEFs known to act downstream of guidance receptors. Thus, we propose that vav acts in coordination with other GEFs to regulate axon growth and guidance during development by linking guidance signals to the cytoskeleton via the modulation of Rac activity.

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Genetic analysis of the Drosophila ellipsoid body neuropil: Organization and development of the central complex

Cited by 81 publications

References 23 publications

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

The Guanine Exchange FactorvavControls Axon Growth and Guidance duringDrosophilaDevelopment

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