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Science 20 December 1996: Vol. 274. no. 5295, pp. 2104 - 2107 DOI: 10.1126/science.274.5295.2104
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Reports
Associative Learning Disrupted by Impaired Gs
Signaling in Drosophila Mushroom Bodies
John B. Connolly,
*
Ian J. H. Roberts,
J.
Douglas Armstrong,
Kim Kaiser,
Michael Forte,
Tim Tully,
Cahir J. O'Kane
Disruptions in mushroom body (MB) or central complex (CC) brain
structures impair Drosophila associative olfactory learning. Perturbations in adenosine 3 ,5 monophosphate signaling also disrupt
learning. To integrate these observations, expression of a
constitutively activated stimulatory heterotrimeric guanosine triphosphate-binding protein subunit (G s*) was
targeted to these brain structures. The ability to associate odors with
electroshock was abolished when G s* was targeted to MB,
but not CC, structures, whereas sensorimotor responses to these stimuli
remained normal. Expression of G s* did not affect gross
MB morphology, and wild-type G s expression did not
affect learning. Thus, olfactory learning depends on regulated
Gs signaling in Drosophila MBs.
J. B. Connolly, Cold Spring Harbor Laboratory, Cold Spring Harbor,
NY 11724, USA, and Department of Genetics, University of Cambridge,
Cambridge, CB2 3EH, UK.
I. J. H. Roberts and C. J. O'Kane. Department of Genetics, University
of Cambridge, Cambridge, CB2 3EH, UK.
J. D. Armstrong and K. Kaiser, Division of Molecular Genetics,
Institute of Biomedical and Life Sciences, Pontecorvo Building,
University of Glasgow, Glasgow, G11 6NU, UK.
M. Forte, Vollum Institute for Advanced Biomedical Research, Oregon
Health Sciences University, 3181 Southwestern Sam Jackson Park Road,
Portland, OR 97201, USA.
T. Tully, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
*
To whom correspondence should be addressed. E-mail:
connollj{at}cshl.org
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- loco encodes an RGS protein required for Drosophila glial differentiation.
- S Granderath, A Stollewerk, S Greig, C. Goodman, C. O'Kane, and C Klambt (1999)
Development
126, 1781-1791
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- The Steroid Hormone 20-Hydroxyecdysone Enhances Neurite Growth of Drosophila Mushroom Body Neurons Isolated during Metamorphosis.
- R. Kraft, R. B. Levine, and L. L. Restifo (1998)
J. Neurosci.
18, 8886-8899
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- A Novel Octopamine Receptor with Preferential Expression in Drosophila Mushroom Bodies.
- K.-A. Han, N. S. Millar, and R. L. Davis (1998)
J. Neurosci.
18, 3650-3658
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- What Do the Mushroom Bodies Do for the Insect Brain? An Introduction.
- M. Heisenberg (1998)
Learn. Mem.
5, 1-10
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- Evolution, Discovery, and Interpretations of Arthropod Mushroom Bodies.
- N. J. Strausfeld, L. Hansen, Y. Li, R. S. Gomez, and K. Ito (1998)
Learn. Mem.
5, 11-37
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- The Organization of Extrinsic Neurons and Their Implications in the Functional Roles of the Mushroom Bodies in Drosophila melanogaster Meigen.
- K. Ito, K. Suzuki, P. Estes, M. Ramaswami, D. Yamamoto, and N. J. Strausfeld (1998)
Learn. Mem.
5, 52-77
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- Metamorphosis of the Mushroom Bodies; Large-Scale Rearrangements of the Neural Substrates for Associative Learning and Memory in Drosophila.
- J. D. Armstrong, J. S. de Belle, Z. Wang, and K. Kaiser (1998)
Learn. Mem.
5, 102-114
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- Dopamine and Mushroom Bodies in Drosophila: Experience-Dependent and -Independent Aspects of Sexual Behavior.
- W. S. Neckameyer (1998)
Learn. Mem.
5, 157-165
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- Drosophila Mushroom Bodies Are Dispensable for Visual, Tactile, and Motor Learning.
- R. Wolf, T. Wittig, L. Liu, G. Wustmann, D. Eyding, and M. Heisenberg (1998)
Learn. Mem.
5, 166-178
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- Mushroom Bodies Suppress Locomotor Activity in Drosophila melanogaster.
- J.-R. Martin, R. Ernst, and M. Heisenberg (1998)
Learn. Mem.
5, 179-191
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- Defective Learning in Mutants of the Drosophila Gene for a Regulatory Subunit of cAMP-Dependent Protein Kinase.
- S. F. Goodwin, M. Del Vecchio, K. Velinzon, C. Hogel, S. R. H. Russell, T. Tully, and K. Kaiser (1997)
J. Neurosci.
17, 8817-8827
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- An activating mutation in a Caenorhabditis elegans Gs protein induces neural degeneration..
- H C Korswagen, J H Park, Y Ohshima, and R H Plasterk (1997)
Genes & Dev.
11, 1493-1503
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- A Return to Genetic Dissection of Memory in Drosophila.
- T. Tully, G. Bolwig, J. Christensen, J. Connolly, M. DelVecchio, J. DeZazzo, J. Dubnau, C. Jones, S. Pinto, M. Regulski, et al. (1996)
Cold Spring Harb Symp Quant Biol
61, 207-218
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- The Role of Drosophila Mushroom Body Signaling in Olfactory Memory.
- S. E. McGuire, P. T. Le, and R. L. Davis (2001)
Science
293, 1330-1333
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- Type II cAMP-dependent Protein Kinase-deficient Drosophila Are Viable but Show Developmental, Circadian, and Drug Response Phenotypes.
- S. K. Park, S. A. Sedore, C. Cronmiller, and J. Hirsh (2000)
J. Biol. Chem.
275, 20588-20596
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