Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons

doi:10.1002/(SICI)1097-4695(199705)32:5<443::AID-NEU1>3.0.CO;2-5

Home
/
Papers
/
Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons

Journal Article•DOI•

Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons

Reinhard F. Stocker¹, Gertrud Heimbeck¹, Nanaë Gendre¹, J S de Belle²•Institutions (2)

University of Fribourg¹, Max Planck Society²

01 May 1997-Journal of Neurobiology (J Neurobiol)-Vol. 32, Iss: 5, pp 443-456

TL;DR: Early larval HU application to P[GAL4] strains that label specific neuron types enabled us to identify the origins of the two major classes of interneurons in the olfactory system and suggested that differentiated RI are present at the larval stage already and may be retained through metamorphosis.

read less

Abstract: Hydroxyurea (HU) treatment of early first instar larvae in Drosophila was previously shown to ablate a single dividing lateral neuroblast (LNb) in the brain. Early larval HU application to P[GAL4] strains that label specific neuron types enabled us to identify the origins of the two major classes of interneurons in the olfactory system. HU treatment resulted in the loss of antennal lobe local interneurons and of a subset of relay interneurons (RI), elements usually projecting to the calyx and the lateral protocerebrum (LPR). Other RI were resistant to HU and still projected to the LPR. However, they formed no collaterals in the calyx region (which was also ablated), suggesting that their survival does not depend on targets in the calyx. Hence, the ablated interneurons were derived from the LNb, whereas the HU-resistant elements originated from neuroblasts which begin to divide later in larval life. Developmental GAL4 expression patterns suggested that differentiated RI are present at the larval stage already and may be retained through metamorphosis.

...read moreread less

Citations

PDF

Open Access

More filters

Journal Article•DOI•

Molecular Architecture of Smell and Taste in Drosophila

[...]

Leslie B. Vosshall¹, Reinhard F. Stocker²•Institutions (2)

Rockefeller University¹, University of Fribourg²

28 Jun 2007-Annual Review of Neuroscience

TL;DR: A critical review of the recent literature in smell and taste studies in Drosophila is provided to provide broad insights into the problem of sensory coding.

...read moreread less

Abstract: The chemical senses—smell and taste—allow animals to evaluate and distinguish valuable food resources from dangerous substances in the environment. The central mechanisms by which the brain recognizes and discriminates attractive and repulsive odorants and tastants, and makes behavioral decisions accordingly, are not well understood in any organism. Recent molecular and neuroanatomical advances in Drosophila have produced a nearly complete picture of the peripheral neuroanatomy and function of smell and taste in this insect. Neurophysiological experiments have begun to provide insight into the mechanisms by which these animals process chemosensory cues. Given the considerable anatomical and functional homology in smell and taste pathways in all higher animals, experimental approaches in Drosophila will likely provide broad insights into the problem of sensory coding. Here we provide a critical review of the recent literature in this field and comment on likely future directions.

...read moreread less

842 citations

Journal Article•DOI•

Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain

[...]

Jing W. Wang¹, Allan M. Wong¹, Jorge Flores¹, Leslie B. Vosshall², Richard Axel¹ - Show less +1 more•Institutions (2)

Howard Hughes Medical Institute¹, Rockefeller University²

24 Jan 2003-Cell

TL;DR: A sensitive imaging system in the Drosophila brain that couples two-photon microscopy with the specific expression of the calcium-sensitive fluorescent protein, G-CaMP is developed, demonstrating that the response pattern of a given glomerulus is a function of the specificity of a single odorant receptor.

...read moreread less

810 citations

Cites background from "Neuroblast ablation in Drosophila P..."

...Or47b-Gal4 (Vosshall et al., 2000), Or43a-Gal4,eral inhibition” is operating in Drosophila, it may exploit Or83b-Gal4, and GH146-Gal4 (Stocker et al., 1997) were used tothe specific connectivity of inhibitory interneurons that drive the expression of UAS-GCaMP or UAS-Or43a.operate across longer relative distances rather than only The osmolarity of adult Drosophila hemolymph is 250 mOsm (Sinon local interneuron circuits. gleton and Woodruff, 1994)....
[...]
...An enhancer trap line, GH146-Gal4, has been characterized that drives the expression of Gal4 in approximately 90 of the 200 PNs (Stocker et al., 1997; Jefferis et al., 2001)....
[...]
...Or47b-Gal4 (Vosshall et al., 2000), Or43a-Gal4,eral inhibition” is operating in Drosophila, it may exploit Or83b-Gal4, and GH146-Gal4 (Stocker et al., 1997) were used tothe specific connectivity of inhibitory interneurons that drive the expression of UAS-GCaMP or UAS-Or43a.operate across longer…...
[...]

Journal Article•DOI•

Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum

[...]

Allan M. Wong¹, Jing W. Wang¹, Richard Axel¹•Institutions (1)

Howard Hughes Medical Institute¹

19 Apr 2002-Cell

TL;DR: In the fruit fly, Drosophila, olfactory sensory neurons expressing a given receptor project to spatially invariant loci in the antennal lobe to create a topographic map of receptor activation, which is represented in higher sensory centers in the brain by projection neurons that innervate the same glomerulus.

...read moreread less

578 citations

Cites background or methods from "Neuroblast ablation in Drosophila P..."

...Larvae containing three transgenes, UAS CD2,y CD8-GFP, Hs-flp, and GH146-Gal4, were given a mild heat shock (32 C forImplications for Sensory Processing 1 hr) at late third instar to remove the FLP-out cassette CD2,y Different odorants elicit spatially defined patterns of gloin a subset of the neurons....
[...]
...These results demonstrate that a topo- projection neurons (Stocker et al., 1997; Jefferis et al., 2001)....
[...]
...In contrast, the linkage distance between a VA1lm dorsal PN and any DA2 PN is and axonal projections were analyzed for 20 individual GH146-Gal4 flies, also bearing the transgenes Hs-flp and UAS CD2,y CD8-GFP, were subjected to mild heat shock during the late larval stage....
[...]
...The concept of the critical period in the mamgenerate samples containing single PNs:malian visual system during which visual input shapes GH146-Gal4 (Stocker et al., 1997); UAS CD2, y CD8-GFP,connectivity does not appear to have an analogous kindly provided by Gary Struhl; UAS-GFPnls (Struhl and…...
[...]
...…used We have examined how olfactory information is repre- an enhancer trap line in which Gal4 is expressed in a subpopulation of projection neurons (Stocker et al., 1997), along with the FLP-out technique (Basler and2 Correspondence: ra27@columbia.edu 3 These authors contributed equally to this…...
[...]

Journal Article•DOI•

Transformation of olfactory representations in the Drosophila antennal lobe.

[...]

Rachel Wilson¹, Glenn C. Turner¹, Gilles Laurent¹•Institutions (1)

California Institute of Technology¹

16 Jan 2004-Science

TL;DR: Comparison of odor-evoked activity from afferents and postsynaptic neurons in the same glomerulus revealed that second-order neurons display broader tuning and more complex responses than their primary afferente, implicating lateral interactions within the antennal lobe.

...read moreread less

Abstract: Molecular genetics has revealed a precise stereotypy in the projection of primary olfactory sensory neurons onto secondary neurons. A major challenge is to understand how this mapping translates into odor responses in these second-order neurons. We investigated this question in Drosophila using whole-cell recordings in vivo. We observe that monomolecular odors generally elicit responses in large ensembles of antennal lobe neurons. Comparison of odor-evoked activity from afferents and postsynaptic neurons in the same glomerulus revealed that second-order neurons display broader tuning and more complex responses than their primary afferents. This indicates a major transformation of odor representations, implicating lateral interactions within the antennal lobe.

...read moreread less

555 citations

Journal Article•DOI•

The Q System: A Repressible Binary System for Transgene Expression, Lineage Tracing, and Mosaic Analysis

[...]

Christopher Potter¹, Bosiljka Tasic², Bosiljka Tasic¹, Emilie V. Russler², Emilie V. Russler¹, Liang Liang¹, Liang Liang², Liqun Luo², Liqun Luo¹ - Show less +5 more•Institutions (2)

Howard Hughes Medical Institute¹, Stanford University²

30 Apr 2010-Cell

TL;DR: The utility of the new repressible binary expression system based on the regulatory genes from the Neurospora qa gene cluster is demonstrated in determining cell division patterns of a neuronal lineage and gene function in cell growth and proliferation, and in dissecting neurons responsible for olfactory attraction.

...read moreread less

538 citations

Cites background from "Neuroblast ablation in Drosophila P..."

...For example, QF driven by the GH146 enhancer (Stocker et al., 1997; Berdnik et al., 2008) drives strong reporter gene expression in olfactory projection neurons (PNs; Figures 2A2, 2A3, 2B2, and 2B3)....
[...]

1
2
3
4
…
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73

Collapse

References

PDF

Open Access

More filters

Journal Article•DOI•

Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.

[...]

Andrea H. Brand¹, Norbert Perrimon¹•Institutions (1)

Harvard University¹

01 Jun 1993-Development

TL;DR: The GAL4 system, a system for targeted gene expression that allows the selective activation of any cloned gene in a wide variety of tissue- and cell-specific patterns, has been designed and used to expand the domain of embryonic expression of the homeobox protein even-skipped.

...read moreread less

Abstract: We have designed a system for targeted gene expression that allows the selective activation of any cloned gene in a wide variety of tissue- and cell-specific patterns. The gene encoding the yeast transcriptional activator GAL4 is inserted randomly into the Drosophila genome to drive GAL4 expression from one of a diverse array of genomic enhancers. It is then possible to introduce a gene containing GAL4 binding sites within its promoter, to activate it in those cells where GAL4 is expressed, and to observe the effect of this directed misexpression on development. We have used GAL4-directed transcription to expand the domain of embryonic expression of the homeobox protein even-skipped. We show that even-skipped represses wingless and transforms cells that would normally secrete naked cuticle into denticle secreting cells. The GAL4 system can thus be used to study regulatory interactions during embryonic development. In adults, targeted expression can be used to generate dominant phenotypes for use in genetic screens. We have directed expression of an activated form of the Dras2 protein, resulting in dominant eye and wing defects that can be used in screens to identify other members of the Dras2 signal transduction pathway.

...read moreread less

9,460 citations

"Neuroblast ablation in Drosophila P..." refers background in this paper

...In contrast, HU activity with a solution containing 5–10 mg X-Gal/mL applied later during larval life dramatically affected dimethylsulfoxide (Brand and Perrimon, 1993)....
[...]
...…larvae aged 24, 48, and 72 h Yet, owing to enhancer trap technology (O’Kane after larval hatching (ALH) were rinsed from the food and Gehring, 1987; Brand and Perrimon, 1993), and transferred to a drop of the HU-containing yeast paste efficient cellular markers can now be generated in a small…...
[...]

Journal Article•DOI•

The Organization of the Chemosensory System in Drosophila Melanogaster: A Review

[...]

Reinhard F. Stocker¹•Institutions (1)

University of Fribourg¹

01 Jan 1994-Cell and Tissue Research

TL;DR: This review surveys the organization of the olfactory and gustatory systems in the imago and in the larva of Drosophila melanogaster, both at the sensory and the central level.

...read moreread less

Abstract: This review surveys the organization of the olfactory and gustatory systems in the imago and in the larva of Drosophila melanogaster, both at the sensory and the central level. Olfactory epithelia of the adult are located primarily on the third antennal segment (funiculus) and on the maxillary palps. About 200 basiconic (BS), 150 trichoid (TS) and 60 coeloconic sensilla (CS) cover the surface of the funiculus, and an additional 60 BS are located on the maxillary palps. Males possess about 30% more TS but 20% fewer BS than females. All these sensilla are multineuronal; they may be purely olfactory or multimodal with an olfactory component. Antennal and maxillary afferents converge onto approximately 35 glomeruli within the antennal lobe. These projections obey precise rules: individual fibers are glomerulus-specific, and different types of sensilla are associated with particular subsets of glomeruli. Possible functions of antennal glomeruli are discussed. In contrast to olfactory sensilla, gustatory sensilla of the imago are located at many sites, including the labellum, the pharynx, the legs, the wing margin and the female genitalia. Each of these sensory sites has its own central target. Taste sensilla are usually composed of one mechano-and three chemosensory neurons. Individual chemosensory neurons within a sensillum respond to distinct subsets of molecules and project into different central target regions. The chemosensory system of the larva is much simpler and consists essentially of three major sensillar complexes on the cephalic lobe, the dorsal, terminal and ventral organs, and a series of pharyngeal sensilla.

...read moreread less

900 citations

Journal Article•DOI•

Detection in situ of genomic regulatory elements in Drosophila.

[...]

Cahir J. O'Kane¹, Walter J. Gehring•Institutions (1)

University of Basel¹

01 Dec 1987-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: The P-lacZ fusion gene is an efficient tool for the recovery of elements that may regulate gene expression in Drosophila and for the generation of a wide variety of cell-type-specific markers.

...read moreread less

Abstract: We have developed an approach for the in situ detection of genomic elements that regulate transcription zin Drosophila melanogaster. The approach is analogous to a powerful method of bacterial genetics, the random generation of operon fusions, that enables the isolation and characterization of genes simply by knowing or postulating their pattern of expression; it is not necessary initially to screen for mutant phenotypes. To apply this approach to Drosophila, we have used the expression of the lacZ gene of Escherichia coli from the P-element promoter in germ-line transformant flies to screen for chromosomal elements that can act at a distance to stimulate expression from this apparently weak promoter. Of 49 transformed fly lines obtained, approximately 70% show some type of spatially regulated expression of the lacZ gene in embryos; many of these express lacZ specifically in the nervous system. The P-lacZ fusion gene is, therefore, an efficient tool for the recovery of elements that may regulate gene expression in Drosophila and for the generation of a wide variety of cell-type-specific markers.

...read moreread less

802 citations

Journal Article•DOI•

Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies

[...]

JS de Belle¹, Martin Heisenberg¹•Institutions (1)

University of Würzburg¹

04 Feb 1994-Science

TL;DR: The results demonstrate that MBs mediate associative odor learning in flies, and that adult flies developing without MBs are unable to perform in a classical conditioning paradigm that tests associative learning of odor cues and electric shock.

...read moreread less

Abstract: The corpora pedunculata, or mushroom bodies (MBs), in the brain of Drosophila melanogaster adults consist of approximately 2500 parallel Kenyon cell fibers derived from four MB neuroblasts. Hydroxyurea fed to newly hatched larvae selectively deletes these cells, resulting in complete, precise MB albation. Adult flies developing without MBs behave normally in most respects, but are unable to perform in a classical conditioning paradigm that tests associative learning of odor cues and electric shock. This deficit cannot be attributed to reductions in olfactory sensitivity, shock reactivity, or locomotor behavior. The results demonstrate that MBs mediate associative odor learning in flies.

...read moreread less

787 citations

"Neuroblast ablation in Drosophila P..." refers background or methods in this paper

...Briefly, 50 mg of HU was added ment of the different types of interneurons to partic- to 1 mL of fresh yeast made semiliquid in a microwave ular cell lineages (de Belle and Heisenberg, 1994). oven....
[...]
...…was applied for 4 h at 24 h ALH to line GH146, the AL of the few adults recovered wasagreement with data in the wild-type and other GAL4 lines (de Belle and Heisenberg, 1994; Arm- extremely reduced in size, comprising only 20–30 mm in the longitudinal axis (compared to 55–65strong et al.,…...
[...]
...Thus, even a sigin olfactory learning (Heisenberg et al., 1985; Nigh- nificant loss of target interneurons does not abolish orn et al., 1991; de Belle and Heisenberg, 1994; de glomeruli formation....
[...]
...…serial 4-mm Epon sections. we counted 148 { 3.2 trichoid sensilla per antenna, the corresponding figures for HU-treated fliesAs shown previously (de Belle and Heisenberg, 1994), the AL of HU-treated males and females were 158 { 6.1 (HU at 0 h ALH) , 141 { 3.5 (24 h ALH) , 149 { 7.5 (48 h ALH) ,…...
[...]
...Afterother HU ablation studies using the same protocol (de Belle and Heisenberg, 1994; J.S. de Belle, un- eclosion, LocI showed the mature lacZ pattern, whereas TAU staining was fully established only 2published data) . days later....
[...]

Journal Article•DOI•

Drosophila Mushroom Body Mutants are Deficient in Olfactory Learning

[...]

Martin Heisenberg¹, Alexander Borst¹, Sibylle Wagner, Duncan Byers²•Institutions (2)

Max Planck Society¹, State University of New York System²

01 Feb 1985-Journal of Neurogenetics

TL;DR: Two Drosophila mutants are described in which the connections between the input to and the output from the mushroom bodies is largely interrupted, and the defect seems not to impair learning of color discrimination tasks or operant learning involving visual cues.

...read moreread less

Abstract: Two Drosophila mutants are described in which the connections between the input to and the output from the mushroom bodies is largely interrupted. In all forms of the flies (larva, imago, male, female) showing the structural defect, olfactory conditioning is impaired. Learning is completely abolished when electroshock is used as reinforcement and partially suppressed in reward learning with sucrose. No influence of the mushroom body defect on the perception of the conditioning stimuli or on spontaneous olfactory behavior is observed. The defect seems not to impair learning of color discrimination tasks or operant learning involving visual cues.

...read moreread less

694 citations