Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Advertising
    • Feedback
    • For library administrators
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Advertising
    • Feedback
    • For library administrators
JOURNAL ARTICLES
Early development of the Drosophila mushroom body: the roles of eyeless and dachshund
A. Noveen, A. Daniel, V. Hartenstein
Development 2000 127: 3475-3488;
A. Noveen
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
A. Daniel
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
V. Hartenstein
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

The mushroom body (MB) is a uniquely identifiable brain structure present in most arthropods. Functional studies have established its role in learning and memory. Here we describe the early embryonic origin of the four neuroblasts that give rise to the mushroom body and follow its morphogenesis through later embryonic stages. In the late embryo, axons of MB neurons lay down a characteristic pattern of pathways. eyeless (ey) and dachshund (dac) are expressed in the progenitor cells and neurons of the MB in the embryo and larva. In the larval brains of the hypomorphic ey(R) strain, we find that beside an overall reduction of MB neurons, one MB pathway, the medial lobe, is malformed or missing. Overexpression of eyeless in MBs under the control of an MB-specific promoter results in a converse type of axon pathway abnormality, i.e. malformation or loss of the dorsal lobe. In contrast, loss of dachshund results in deformation of the dorsal lobe, whereas no lobe abnormalities can be detected following dachshund overexpression. These results indicate that ey and dachshund may have a role in axon pathway selection during embryogenesis.

REFERENCES

    1. Altmann C. R.,
    2. Chow R. L.,
    3. Lang R. A.,
    4. Hemmati-Brivanlou A.
    (1997) Lens induction by Pax-6 in Xenopus laevis. Dev. Biol 185, 119–123
    OpenUrlCrossRefPubMedWeb of Science
    1. Bonini N. M.,
    2. Bui Q. T.,
    3. Gray-Board G. L.,
    4. Warrick J. M.
    (1997) The Drosophila eyes absent gene directs ectopic eye formation in a pathway conserved between flies and vertebrates. Development 124, 4819–4826
    OpenUrlAbstract
    1. Bonkowsky J. L.,
    2. Yoshikawa S.,
    3. O'Keefe D. D.,
    4. Scully A. L.,
    5. Thomas J. B.
    (1999) Axon routing across the midline controlled by the Drosophila Derailed receptor. Nature 402, 540–544
    OpenUrlCrossRefPubMed
    1. Callaerts P.,
    2. Halder G.,
    3. Gehring W. J.
    (1997) PAX-6 in development and evolution. Annu. Rev. Neurosci 20, 483–532
    OpenUrlCrossRefPubMedWeb of Science
    1. Callahan C. A.,
    2. Muralidhar M. G.,
    3. Lundgren S. E.,
    4. Scully A. L.,
    5. Thomas J. B.
    (1995) Control of neuronal pathway selection by a Drosophila receptor protein-tyrosine kinase family member. Nature 376, 171–174
    OpenUrlCrossRefPubMed
    1. Caric D.,
    2. Gooday D.,
    3. Hill R. E.,
    4. McConnell S. K.,
    5. Price D. J.
    (1997) Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax-6. Development 124, 5087–5096
    OpenUrlAbstract
    1. Caubit X.,
    2. Thangarajah R.,
    3. Theil T.,
    4. Wirth J.,
    5. Nothwang H. G.,
    6. Ruther U.,
    7. Krauss S.
    (1999) Mouse Dac, a novel nuclear factor with homology to Drosophila dachshund shows a dynamic expression in the neural crest, the eye, the neocortex, and the limb bud. Dev. Dyn 214, 66–80
    OpenUrlCrossRefPubMedWeb of Science
    1. Chapouton P.,
    2. Gartner A.,
    3. Gotz M.
    (1999) The role of Pax6 in restricting cell migration between developing cortex and basal ganglia. Development 126, 5569–5579
    OpenUrlAbstract
    1. Chen R.,
    2. Amoui M.,
    3. Zhang Z.,
    4. Mardon G.
    (1997) dachshund and eyes absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell 91, 893–903
    OpenUrlCrossRefPubMedWeb of Science
    1. Chen R.,
    2. Halder G.,
    3. Zhang Z.,
    4. Mardon G.
    (1999) Signaling by the TGF-beta homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila. Development 126, 935–943
    OpenUrlAbstract
    1. Cheyette B. N.,
    2. Green P. J.,
    3. Martin K.,
    4. Garren H.,
    5. Hartenstein V.,
    6. Zipursky S. L.
    (1994) The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12, 977–996
    OpenUrlCrossRefPubMedWeb of Science
    1. Chow R. L.,
    2. Altmann C. R.,
    3. Lang R. A.,
    4. Hemmati-Brivanlou A.
    (1999) Pax6 induces ectopic eyes in a vertebrate. Development 126, 4213–4222
    OpenUrlAbstract
    1. Collinson J. M.,
    2. Hill R. E.,
    3. West J. D.
    (2000) Different roles for Pax6 in the optic vesicle and facial epithelium mediate early morphogenesis of the murine eye. Development 127, 945–956
    OpenUrlAbstract
    1. Curtiss J.,
    2. Mlodzik M.
    (2000) Morphogenetic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent. Development 127, 1325–1336
    OpenUrlAbstract
    1. Czerny T.,
    2. Halder G.,
    3. Kloter U.,
    4. Souabni A.,
    5. Gehring W. J.,
    6. Busslinger M.
    (1999) twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol. Cell 3, 297–307
    OpenUrl
    1. Daniel A.,
    2. Dumstrei K.,
    3. Lengyel J.,
    4. Hartenstein V.
    (1999) tailless and atonal control cell fate in the embryonic visual system. Development 126, 2945–2954
    OpenUrlAbstract
    1. Davis R. L.
    (1996) Physiology and biochemistry of Drosophila learning mutants. Physiol. Rev 76, 299–317
    OpenUrlAbstract/FREE Full Text
    1. de Belle J.S.,
    2. Heisenberg M.
    (1994) Associative odor learning in Drosophila ablolished by chemical ablation of mushroom bodies. Science 263, 692–695
    OpenUrlAbstract/FREE Full Text
    1. de Belle J. S.,
    2. Heisenberg M.
    (1996) Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). Proc. Natl. Acad. Sci.USA 93, 9875–9880
    OpenUrlAbstract/FREE Full Text
    1. Engelkamp D.,
    2. Rashbass P.,
    3. Seawright A.,
    4. van Heyningen V.
    (1999) Role of Pax6 in development of the cerebellar system. Development 126, 3585–3596
    OpenUrlAbstract
    1. Ericson J.,
    2. Rashbass P.,
    3. Schedl A.,
    4. Brenner-Morton S.,
    5. Kawakami A.,
    6. van Heyningen V.,
    7. Jessell T. M.,
    8. Briscoe J.
    (1997) Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169–180
    OpenUrlCrossRefPubMedWeb of Science
    1. Ferveur J. F.,
    2. Stortkuhl K. F.,
    3. Stocker R. F.,
    4. Greenspan R. J.
    (1995) Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267, 902–905
    OpenUrlAbstract/FREE Full Text
    1. Gehring W. J.,
    2. Ikeo K.
    (1999) Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet 15, 371–377
    OpenUrlCrossRefPubMedWeb of Science
    1. Grenningloh G.,
    2. Rehm E. J.,
    3. Goodman C. S.
    (1991) Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67, 45–57
    OpenUrlCrossRefPubMedWeb of Science
    1. Grindley J. C.,
    2. Hargett L. K.,
    3. Hill R. E.,
    4. Ross A.,
    5. Hogan B. L.
    (1997) Disruption of PAX6 function in mice homozygous for the Pax6Sey-1Neu mutation produces abnormalities in the early development and regionalization of the diencephalon. Mech. Dev 64, 111–126
    OpenUrlCrossRefPubMedWeb of Science
    1. Gotz M.,
    2. Stoykova A.,
    3. Gruss P.
    (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031–1044
    OpenUrlCrossRefPubMedWeb of Science
    1. Halder G.,
    2. Callaerts P.,
    3. Flister S.,
    4. Walldorf U.,
    5. Kloter U.,
    6. Gehring W. J.
    (1998) Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125, 2181–2191
    OpenUrlAbstract
    1. Hammond K. L.,
    2. Hanson I. M.,
    3. Brown A. G.,
    4. Lettice L. A.,
    5. Hill R. E.
    (1998) Mammalian and Drosophiladachshund genes are related to the Ski proto-oncogene and are expressed in eye and limb. Mech. Dev 74, 121–131
    OpenUrlCrossRefPubMedWeb of Science
    1. Hanson I.,
    2. van Heyningen V.
    (1995) Pax6: more than meets the eye. Trends Genet 11, 268–272
    OpenUrlCrossRefPubMedWeb of Science
    1. Hartenstein V.,
    2. Younossi-Hartenstein A.,
    3. Lekven A.
    (1994) Delamination and division in the Drosophila neurectoderm: Spatio-temporal pattern, cytoskeletal dynamics, and common control by neurogenic and segment polarity genes. Dev. Biol 165, 480–499
    OpenUrlCrossRefPubMedWeb of Science
    1. Hazelett D. J.,
    2. Bourouis M.,
    3. Walldorf U.,
    4. Treisman J. E.
    (1998) decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125, 3741–3751
    OpenUrlAbstract
    1. Heanue T. A.,
    2. Reshef R.,
    3. Davis R. J.,
    4. Mardon G.,
    5. Oliver G.,
    6. Tomarev S.,
    7. Lassar A. B.,
    8. Tabin C. J.
    (1999) Synergistic regulation of vertebrate muscle development by dach2, eya2, and six1, homologs of genes required for Drosophila eye formation. Genes Dev 13, 3231–3243
    OpenUrlAbstract/FREE Full Text
    1. Heisenberg M.
    (1980) Mutants of brain structure and function: what is the significance of the mushroom bodies for behavior?. Basic Life Sci 16, 373–390
    OpenUrlPubMed
    1. Heisenberg M.,
    2. Borst A.,
    3. Wagner S.,
    4. Byers D.
    (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogen 2, 1–30
    OpenUrlCrossRefPubMedWeb of Science
    1. Hill R. E.,
    2. Favor J.,
    3. Hogan B. L.,
    4. Ton C. C.,
    5. Saunders G. F.,
    6. Hanson I. M.,
    7. Prosser J.,
    8. Jordan T.,
    9. Hastie N. D.,
    10. van Heyningen V.
    (1991) Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522–525
    OpenUrlCrossRefPubMedWeb of Science
    1. Hoge M. A.
    (1915) Another gene in the fourth chromosome of Drosophila. Am. Nat 49, 47–.
    OpenUrl
    1. Holst B. D.,
    2. Wang Y.,
    3. Jones F. S.,
    4. Edelman G. M.
    (1997) A binding site for Pax proteins regulates expression of the gene for the neural cell adhesion molecule in the embryonic spinal cord. Proc. Natl. Acad. Sci. USA 94, 1465–1470
    OpenUrlAbstract/FREE Full Text
    1. Ito K.,
    2. Awano W.,
    3. Suzuki K.,
    4. Hiromi Y.,
    5. Yamamoto D.
    (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124, 761–771
    OpenUrlAbstract
    1. Ito K.,
    2. Hotta Y.
    (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophilamelanogaster. Dev. Biol 149, 134–148
    OpenUrlCrossRefPubMedWeb of Science
    1. Ito K.,
    2. Sass H.,
    3. Urban J.,
    4. Hofbauer A.,
    5. Schneuwly S.
    (1997) GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 290, 1–10
    OpenUrlCrossRefPubMedWeb of Science
    1. Kawano H.,
    2. Fukuda T.,
    3. Kubo K.,
    4. Horie M.,
    5. Uyemura K.,
    6. Takeuchi K.,
    7. Osumi N.,
    8. Eto K.,
    9. Kawamura K.
    (1999) Pax-6 is required for thalamocortical pathway formation in fetal rats. J. Comp. Neurol 408, 147–160
    OpenUrlCrossRefPubMedWeb of Science
    1. Kioussi C.,
    2. O'Connell S.,
    3. St-Onge L.,
    4. Treier M.,
    5. Gleiberman A. S.,
    6. Gruss P.,
    7. Rosenfeld M. G.
    (1999) Pax6 is essential for establishingventral-dorsal cell boundaries in pituitary gland development. Proc. Natl. Acad. Sci. USA 96, 14378–14382
    OpenUrlAbstract/FREE Full Text
    1. Kurusu M.,
    2. Nagao T.,
    3. Walldorf U.,
    4. Flister S.,
    5. Gehring W. J.,
    6. Furukubo-Tokunaga K.
    (2000) Genetic control of development of the mushroom bodies, the associative learning centers in the Drosophila brain, by the eyeless, twin of eyeless, and dachshund genes. Proc. Natl. Acad. Sci. USA 97, 2140–2144
    OpenUrlAbstract/FREE Full Text
    1. Lee T.,
    2. Lee A.,
    3. Luo L.
    (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126, 4065–4076
    OpenUrlAbstract
    1. Lee T.,
    2. Luo L.
    (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Liu L.,
    2. Wolf R.,
    3. Ernst R.,
    4. Heisenberg M.
    (1999) Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400, 753–756
    OpenUrlCrossRefPubMedWeb of Science
    1. Loosli F.,
    2. Winkler S.,
    3. Wittbrodt J.
    (1999) Six3 overexpression initiates the formation of ectopic retina. Genes Dev 13, 649–654
    OpenUrlAbstract/FREE Full Text
    1. Mardon G.,
    2. Solomon N. M.,
    3. Rubin G. M.
    (1994) dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120, 3473–3486
    OpenUrlAbstract
    1. Martini S. R.,
    2. Roman G.,
    3. Meuser S.,
    4. Mardon G.,
    5. Davis R. L.
    (2000) The retinal determination gene, dachshund, is required for mushroom body cell differentiation. Development 127, 2663–2672
    OpenUrlAbstract
    1. Mastick G. S.,
    2. Davis N. M.,
    3. Andrew G. L.,
    4. Easter S. S., Jr
    (1997) Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain. Development 124, 1985–1997
    OpenUrlAbstract
    1. McBride S. M.,
    2. Giuliani G.,
    3. Choi C.,
    4. Krause P.,
    5. Correale D.,
    6. Watson K.,
    7. Baker G.,
    8. Siwicki K. K.
    (1999) Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24, 967–977
    OpenUrlCrossRefPubMedWeb of Science
    1. Meech R.,
    2. Kallunki P.,
    3. Edelman G. M.,
    4. Jones F. S.
    (1999) A binding site for homeodomain and Pax proteins is necessary for L1 cell adhesion molecule gene expression by Pax-6 and bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA 96, 2420–2425
    OpenUrlAbstract/FREE Full Text
    1. Melzig J.,
    2. Rein K. H.,
    3. Schafer U.,
    4. Pfister H.,
    5. Jackle H.,
    6. Heisenberg M.,
    7. Raabe T.
    (1998) A protein related to p21-activated kinase (PAK) that is involved in neurogenesis in the Drosophila adult central nervous system. Curr. Biol 8, 1223–1226
    OpenUrlCrossRefPubMedWeb of Science
    1. Moreau-Fauvarque C.,
    2. Taillebourg E.,
    3. Boissoneau E.,
    4. Mesnard J.,
    5. Dura J. M.
    (1998) The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mech. Dev 78, 47–61
    OpenUrlCrossRefPubMedWeb of Science
    1. Nassif C.,
    2. Noveen A.,
    3. Hartenstein V.
    (1998) Embryonic development of the Drosophila brain I. the pattern of pioneer tracts. J. Comp. Neurol 402, 10–31
    OpenUrlCrossRefPubMedWeb of Science
    1. Nguyen H. T.,
    2. Bodmer R.,
    3. Abmayr S. M.,
    4. McDermott J. C.,
    5. Spoerel N. A.
    (1994) D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc. Natl. Acad. Sci. USA 91, 7520–7524
    OpenUrlAbstract/FREE Full Text
    1. O'Dell K. M.,
    2. Armstrong J. D.,
    3. Yang M. Y.,
    4. Kaiser K.
    (1995) Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15, 55–61
    OpenUrlCrossRefPubMedWeb of Science
    1. Ohto H.,
    2. Kamada S.,
    3. Tago K.,
    4. Tominaga S. I.,
    5. Ozaki H.,
    6. Sato S.,
    7. Kawakami K.
    (1999) Cooperation of six and eya in activation of their target genes through nuclear translocation of Eya. Mol. Cel. Biol 19, 6815–6824
    OpenUrlAbstract/FREE Full Text
    1. Osumi N.,
    2. Hirota A.,
    3. Ohuchi H.,
    4. Nakafuku M.,
    5. Iimura T.,
    6. Kuratani S.,
    7. Fujiwara M.,
    8. Noji S.,
    9. Eto K.
    (1997) Pax-6 is involved in the specification of hindbrain motor neuron subtype. Development 124, 2961–2972
    OpenUrlAbstract
    1. Pan D.,
    2. Rubin G. M.
    (1998) Targeted expression of teashirt induces ectopic eyes in Drosophila. Proc. Natl. Acad. Sci. USA 95, 15508–15512
    OpenUrlAbstract/FREE Full Text
    1. Pignoni F.,
    2. Hu B.,
    3. Zavitz K. H.,
    4. Xiao J.,
    5. Garrity P. A.,
    6. Zipursky S. L.
    (1997) The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell 91, 881–891
    OpenUrlCrossRefPubMedWeb of Science
    1. Pignoni F.,
    2. Zipursky S. L.
    (1997) Induction of Drosophila eye development by decapentaplegic. Development 124, 271–278
    OpenUrlAbstract
    1. Prokop A.,
    2. Technau G. M.
    (1991) The origin of postembryonicneuroblasts in the ventral nerve cord of Drosophilamelanogaster. Development 111, 79–88
    OpenUrlAbstract
    1. Prokop A.,
    2. Technau G. M.
    (1994) Normal function of the mushroom body defect gene of Drosophila is required for the regulation of the number and proliferation of neuroblasts. Dev. Biol 161, 321–337
    OpenUrlCrossRefPubMedWeb of Science
    1. Quinn J. C.,
    2. West J. D.,
    3. Hill R. E.
    (1996) Multiple functions for Pax6 in mouse eye and nasal development. Genes Dev 10, 435–446
    OpenUrlAbstract/FREE Full Text
    1. Quiring R.,
    2. Walldorf U.,
    3. Kloter U.,
    4. Gehring W. J.
    (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in human. Science 265, 785–789
    OpenUrlAbstract/FREE Full Text
    1. Schedl A.,
    2. Ross A.,
    3. Lee M.,
    4. Engelkamp D.,
    5. Rashbass P.,
    6. van Heyningen V.,
    7. Hastie N. D.
    (1996) Influence of PAX6 gene dosage on development: overexpression causes severe eye abnormalities. Cell 86, 71–82
    OpenUrlCrossRefPubMedWeb of Science
    1. Schulz R. A.,
    2. Chromey C.,
    3. Lu M.-F.,
    4. Zhao B.,
    5. Olson E. N.
    (1996) Expression of the D-MEF2 transcription factor in the Drosophila brain suggests a role in neuronal cell differentiation. Oncogene 12, 1827–1831
    OpenUrlPubMedWeb of Science
    1. Shen W.,
    2. Mardon G.
    (1997) Ectopic eye development in Drosophila induced by directed dachshund expression. Development 124, 45–52
    OpenUrlAbstract
    1. Skeath J. B.,
    2. Carroll S. B.
    (1992) Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114, 939–946
    OpenUrlAbstract
    1. Skoulakis E. M.,
    2. Davis R. L.
    (1996) Olfactory learning deficits in mutants for leonardo, a Drosophila gene encoding a 14–3-3 protein. Neuron 17, 931–944
    OpenUrlCrossRefPubMedWeb of Science
    1. Skoulakis E. M.,
    2. Kalderon D.,
    3. Davis R. L.
    (1993) Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11, 197–208
    OpenUrlCrossRefPubMedWeb of Science
    1. Stoykova A.,
    2. Fritsch R.,
    3. Walther C.,
    4. Gruss P.
    (1996) Forebrain patterning defects in Small eye mutant mice. Development 122, 3453–3465
    OpenUrlAbstract
    1. Stoykova A.,
    2. Gotz M.,
    3. Gruss P.,
    4. Price J.
    (1997) Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124, 3765–3777
    OpenUrlAbstract
    1. Struhl G.,
    2. Fitzgerald K.,
    3. Greenwald I.
    (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74, 331–345
    OpenUrlCrossRefPubMedWeb of Science
    1. Technau G. M.,
    2. Heisenberg M.
    (1982) Neural reorganisation during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295, 405–407
    OpenUrlCrossRefPubMed
    1. Ton C. C.,
    2. Hirvonen H.,
    3. Miwa H.,
    4. Weil M. M.,
    5. Monaghan P.,
    6. Jordan T.,
    7. van Heyningen V.,
    8. Hastie N. D.,
    9. Meijers-Heijboer H.,
    10. Drechsler M.,
    11. Royer-Pokora B.,
    12. Collins F.,
    13. Swaroop A.,
    14. Strong L. C.,
    15. Saunders G. F.
    (1991) Positional cloning and characterization of a paired box-and homeobox-containing gene from the Aniridia region. Cell 67, 1059–1074
    OpenUrlCrossRefPubMedWeb of Science
    1. Treisman J. E.
    (1999) A conserved blueprint for the eye?. BioEssays 21, 843–850
    OpenUrlCrossRefPubMedWeb of Science
    1. Walther C.,
    2. Gruss P.
    (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435–1449
    OpenUrlAbstract
    1. Warren N.,
    2. Caric D.,
    3. Pratt T.,
    4. Clausen J. A.,
    5. Asavaritikrai P.,
    6. Mason J. O.,
    7. Hill R. E.,
    8. Price D. J.
    (1999) The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex. Cereb. Cortex 9, 627–635
    OpenUrlAbstract/FREE Full Text
    1. Warren N.,
    2. Price D. J.
    (1997) Roles of Pax-6 in murine diencephalic development. Development 124, 1573–1582
    OpenUrlAbstract
    1. Xu P. X.,
    2. Adams J.,
    3. Peters H.,
    4. Brown M. C.,
    5. Heaney S.,
    6. Maas R.
    (1999) Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nat. Genet 23, 113–117
    OpenUrlCrossRefPubMedWeb of Science
    1. Xu P. X.,
    2. Woo I.,
    3. Her H.,
    4. Beier D. R.,
    5. Maas R. L.
    (1997) Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. Development 124, 219–231
    OpenUrlAbstract
    1. Xu P. X.,
    2. Zhang X.,
    3. Heaney S.,
    4. Yoon A.,
    5. Michelson A. M.,
    6. Maas R. L.
    (1999) Regulation of Pax6 expression is conserved between mice and flies. Development 126, 383–395
    OpenUrlAbstract
    1. Yang M. Y.,
    2. Armstrong J. D.,
    3. Vilinsky I.,
    4. Strausfeld N. J.,
    5. Kaiser K.
    (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15, 45–54
    OpenUrlCrossRefPubMedWeb of Science
    1. Younossi-Hartenstein A.,
    2. Nassif C.,
    3. Hartenstein V.
    (1996) Early neurogenesis of the Drosophila brain. J. Comp. Neur 370, 313–329
    OpenUrlCrossRefPubMedWeb of Science
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Early development of the Drosophila mushroom body: the roles of eyeless and dachshund
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
JOURNAL ARTICLES
Early development of the Drosophila mushroom body: the roles of eyeless and dachshund
A. Noveen, A. Daniel, V. Hartenstein
Development 2000 127: 3475-3488;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
Early development of the Drosophila mushroom body: the roles of eyeless and dachshund
A. Noveen, A. Daniel, V. Hartenstein
Development 2000 127: 3475-3488;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Non-imprinted Igf2r expression decreases growth and rescues the Tme mutation in mice
  • REF-1, a protein with two bHLH domains, alters the pattern of cell fusion in C. elegans by regulating Hox protein activity
  • Centrosome migration into the Drosophila oocyte is independent of BicD and egl, and of the organisation of the microtubule cytoskeleton
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.


Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.


New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.


Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.


Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.


Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.

Articles

  • Accepted manuscripts
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback
  • Institutional usage stats (logged-in users only)

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992