Information de reference pour ce titreAccession Number: | 00009017-200102000-00015.
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Author: | Osborne, Kathleen A. 1,2,3; de Belle, J. Steven 1; Sokolowski, Marla B. 2
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Institution: | (1)Department of Biological Sciences, University of Nevada, Las Vegas, NV 89154, USA (2)Department of Zoology, University of Toronto, Mississauga, Ontario, Canada L5L 1C6
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Title: | Foraging Behaviour in Drosophila Larvae: Mushroom Body Ablation.[Report]
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Source: | Chemical Senses. 26(2):223-230, February 2001.
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Abstract: | Drosophila larvae and adults exhibit a naturally occurring genetically based behavioural polymorphism in locomotor activity while foraging. Larvae of the rover morph exhibit longer foraging trails than sitters and forage between food patches, while sitters have shorter foraging trails and forage within patches. This behaviour is influenced by levels of cGMP-dependent protein kinase (PKG) encoded by the foraging (for) gene. Rover larvae have higher expression levels and higher PKG activities than do sitters. Here we discuss the importance of the for gene for studies of the mechanistic and evolutionary significance of individual differences in behaviour. We also show how structure-function analysis can be used to investigate a role for mushroom bodies in larval behaviour both in the presence and in the absence of food. Hydroxyurea fed to newly hatched larvae prevents the development of all post-embryonically derived mushroom body (MB) neuropil. This method was used to ablate MBs in rover and sitter genetic variants of foraging to test whether these structures mediate expression of the foraging behavioural polymorphism. We found that locomotor activity levels during foraging of both the rover and sitter larval morphs were not significantly influenced by MB ablation. Alternative hypotheses that may explain how variation in foraging behaviour is generated are discussed.
(C) Copyright Oxford University Press 2001.
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References: | Armstrong, J.D., de Belle, J.S., Wang, Z. and Kaiser, K. (1998) Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learn. Mem., 5, 102-114.
Bell, W.J. (1990) Searching behavior patterns in insects. Annu. Rev. Entomol., 35, 447-467.
Benzer, S. (1967) Behavioral mutants of Drosophila isolated by counter-current distribution. Proc. Natl Acad. Sci. USA, 58, 1112-1119.
Connolly, J.B., Roberts, I.J.H., Armstrong, J.D., Kaiser K., Forte, M., Tully, T. and O'Kane, C.J. (1996) Associative learning disrupted by impaired G(S) signaling in Drosophila mushroom bodies. Science, 274, 2104-2107.
Crittenden, J.R., Skoulakis, E.M.C., Han, K.-A., Kalderon, D. and Davis, R.L. (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem., 5, 38-51.
de Belle, J.S. and Heisenberg, M. (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science, 263, 692-695.
de Belle, J.S. and 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.
de Belle, J.S. and Kanzaki, R. (1999) Protocerebral olfactory processing. In Hansson, B.S. (ed.), Insect Olfaction. Springer, Stuttgart, pp. 243-281.
de Belle, J.S. and Sokolowski, M.B. (1987) Heredity of rover/sitter: alternative foraging strategies of Drosophila melanogaster larvae. Heredity, 59, 73-83.
de Belle, J.S. and Sokolowski, M.B. (1989) Rover/sitter foraging behavior in Drosophila melanogaster: genetic localization to chromosome-[alpha]L using compound autosomes. J. Insect Behav., 2, 291-299.
de Belle, J.S., Hilliker, A.J. and Sokolowski, M.B. (1989) Genetic localization of foraging (for): a major gene for larval behavior in Drosophila melanogaster. Genetics, 123, 157-163.
de Belle, J.S., Sokolowski, M.B. and Hilliker, A.J. (1993) Genetic analysis of the foraging microregion of Drosophila melanogaster. Genome, 36, 94-101.
Dubnau, J. and T. Tully (1998) Gene discovery in Drosophila: new insights for learning and memory. Annu. Rev. Neurosci., 21, 407-444.
Erber, J., Homberg, U. and Groneberg, W. (1987) Functional roles of the mushroom bodies in insects. In Gupta, A.P. (ed.), Arthropod Brain: Its Evolution, Development, Structure, and Functions. Wiley, New York, pp. 485-511.
Ferveur, J.-F., Stortkuhl, K.F., Stocker, R.F. and Greenspan, R.J. (1995) Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science, 267, 902-905.
Frank, D.A. and Greenberg, M.E. (1994) CREB: a mediator of long-term memory from mollusks to mammals. Cell, 79, 5-8.
Graf, S. and Sokolowski, M.B. (1989) The effect of development, food-patch quality and starvation on Drosophila melanogaster larval foraging behavior. J. Insect Behav., 2, 301-313.
Hall, J.C. (1994) The mating of a fly. Science, 264, 1702-1714.
Hall, J. C. (1998) Molecular nuerogenetics of biological rhythms. J. Neurogenet., 12, 115-181.
Heisenberg, M. (1989) Genetic approach to learning and memory (mnemogenetics) in Drosophila melanogaster. In Rahmann, H. (ed.), Fundamentals of Memory Formation: Neuronal Plasticity and Brain Function. Fischer, Stuttgart, pp. 3-45.
Heisenberg, M. (1994) Central brain function in insects: genetic studies on the mushroom bodies and central complex in Drosophila. In Schildberger, K. and Elsner, N. (eds), Neural Basis of Behavioural Adaptations. Fischer, Stuttgart, pp. 61-79.
Heisenberg, M. (1998) What do the mushroom bodies do for the insect brain? An introduction. Learn. Mem., 5, 1-10.
Heisenberg, M. and Bohl, K. (1979) Isolation of anatomical brain mutants of Drosophila by histological means. Z. Naturforsch., 34c, 143-147.
Heisenberg, M., Borst, A., Wagner, S. and Byers, D. (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet., 2, 1-30.
Ito, K. and Hotta, Y. (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Devl Biol., 149, 134-148.
Ito, K., Awano, W., Suzuki, K., Hiromi, Y. and 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.
Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D. and Strausfeld, N.J. (1998) The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem., 5, 52-77.
Joiner, M.A. and Griffith, L.C. (2000) Visual input regulates circuit configuration in courtship conditioning of Drosophila melanogaster. Learn. Mem., 7, 32-42.
Kalderon, D. and Rubin, G.M. (1989) cGMP-dependent protein kinase genes in Drosophila. J. Biol. Chem., 264, 10738-10748.
Lee, T., Lee, A. and Luo, L. (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development, 126, 4065-4076.
Levin, L.R., Han, P.L., Hwang, P.M., Feinstein, P.G., Havis, R.L. and Reed, R.R. (1992) The Drosophila learning and memory gene rutabaga encodes a Ca2+/calmodulin-responsive adenylyl cyclase. Cell, 68, 479-489.
Liu, L., Wolf, R., Ernst, R. and Heisenberg, M. (1999) Context generalization in Drosophila visual learning requires the mushroom bodies. Nature, 400, 753-756.
Lohmann, S.M., Vaandrager, A.B., Smolenski, A., Walter, U. and DeJonge, H.R. (1997) Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem. Sci., 22, 307-312.
Martin, J.-R., Ernst, R. and Heisenberg, M. (1998) Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn. Mem., 5, 179-191.
Nagle, K.J and Bell, W.J. (1987) Genetic control of the search tactic of Drosophila melanogaster: an ethometric analysis of rover/sitter traits in adult flies. Behav. Genet., 17, 385-408.
Neckameyer, W.S. (1998) Dopamine and mushrooom bodies in Drosophila: experience-dependent and -independent aspects of sexual behavior. Learn. Mem., 5, 156-165.
Nighorn, A., Healy, M.J. and Davis, R.L. (1991) The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron, 6, 455-467.
O'Dell, K.M.C., Armstrong, J.D., Yang, M.Y. and Kaiser, K. (1995) Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron, 15, 55-61.
Osborne, K.A., Robichon, A., Burgess, E., Butland, S., Shaw, R.A., Coulthard, A., Pereira, H.S., Greenspan, R.J. and Sokolowski, M.B. (1997) Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science, 277, 834-836.
Pennisi E. (1997) What makes fruit flies roam? Science, 277, 763-764.
Pereira, H.S. and Sokolowski, M.B. (1993) Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. Proc. Natl Acad. Sci. USA, 90, 5044-5046.
Pereira, H.S., Macdonald, D.E., Hilliker, A.J. and Sokolowski, M.B. (1995) Chaser (Csr), a new gene affecting larval foraging behaviour in Drosophila melanogaster. Genetics, 140, 263-270.
Prokop, A. and 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. Devl Biol., 161, 321-337.
Renger, J.J., Yao, W.-D., Sokolowski, M.B. and Wu, C.-F. (1999) Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging in Drosophila. J. Neurosci., 19, 1-8.
Ruth, P. (1999) Cyclic GMP-dependent protein kinases: understanding in vivo functions by gene targeting. Pharmacol. Ther., 82, 355-372.
Schurmann, F.-W. (1987) The architecture of the mushroom bodies and related neuropils in the insect brain. In Gupta, A.P. (ed.), Arthropod Brain: Its Evolution, Development, Structure, and Functions. Wiley, New York, pp. 231-264.
Shaver, S.A., Varnam, C.J., Hilliker, A.J. and Sokolowski, M.B. (1998) The foraging gene affects adult but not larval olfactory-related behavior in Drosophila melanogaster. Behav. Brain Res., 95, 23-29.
Skoulakis, E.M.C., Kalderon, D. and 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.
Sokolowski, M. B. (1980) Foraging strategies of Drosophila melanogaster: a chromosomal analysis. Behav. Genet., 10, 291-302.
Sokolowski, M. B. (1998) Genes for normal behavioral variation: recent clues from flies and worms. Neuron, 21, 1-4.
Sokolowski, M. B. and Hansell, K.P. (1992) The foraging locus: behavioral tests for normal muscle movement in rover and sitter Drosophila melanogaster larvae. Genetica, 85, 205-209.
Sokolowski, M.B. and Riedl, C. (1999) Behaviour-genetic and molecular analysis of naturally occurring variation in Drosophila larval foraging behaviour. In Gerlai, R. and Crusio, W. (eds), Molecular-genetic Techniques for Brain and Behaviour. Elsevier, London, pp. 517-532.
Sokolowski, M.B., Kent, C. and Wong, J. (1984) Drosophila larval foraging behaviour: developmental stages. Anim. Behav, 32, 645-651.
Sokolowski, M.B., Pereira, H.S. and Hughes, K. (1997) Evolution of foraging behavior in Drosophila by density-dependent selection. Proc. Natl Acad. Sci. USA, 94, 7373-7377.
Stocker, R.F. (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res., 275, 3-26.
Stocker, R.F., Heimbeck, G., Gendre, N. and de Belle, J.S. (1997) Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of antennal target interneurons. J. Neurobiol., 32, 443-456.
Stocker, R.F., Leinhard, M.C., Borst, A. and Fischbach, K.-F. (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res., 262, 9-34.
Strausfeld, N.J. (1976) Atlas of an Insect Brain. Springer, Heidelberg.
Strausfeld, N.J., Hansen, L., Li, Y., Gomez, R.S. and Ito, K. (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn. Mem., 5, 11-37.
Strauss, R. and Heisenberg, M. (1993) A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci., 13, 1852-1861.
Strauss, R., Hanesch, U., Kinkelin, M., Wolf, R. and Heisenberg, M. (1992) no-bridge of Drosophila melanogaster: portrait of a structural brain mutant of the central complex. J. Neurogenet., 8, 125-155.
Sweeney, T.S., Hidalgo, A., de Belle, J.S. and Keshishian, H. (2000) Functional ablation. In Sullivan, B., Ashburner, M. and Hawley, S. (eds), Drosophila Protocols. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 449-477.
Technau, G.M. (1983) Die entwicklung der Corpora Pedunculata von Drosophila melanogaster. Doctoral thesis, University of Wurzburg.
Technau, G.M. and Heisenberg, M. (1982) Neural reorganisation during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature, 295, 405-407.
Tettamanti, M., Armstrong, J.D., Endo, K., Furokubo-Tokunaga, K., Kaiser, K. and Reichert, H. (1997) Analysis of mushroom body development by enhancer-trap expression patterns in the Drosophila brain. Devl Genes Evol., 207, 242-252.
Tortorici, C. and Bell, W.J. (1988) Search orientation in adult Drosophila melanogaster: responses of rovers and sitters to resource dispersion in a food patch. J. Insect Behav., 1, 209-224.
Truman, J.W. and Bate, M. (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Devl Biol., 125, 145-157.
Tully, T. and Quinn, W.G. (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol., 157, 263-277.
Varnam, C.J., Strauss, R., de Belle, J.S. and Sokolowski, M.B. (1996) Larval behavior of central complex mutants in Drosophila melanogaster: interactions between no bridge, foraging and Chaser. J. Neurogenet., 11, 99-115.
Wang, X. and Robinson, P.J. (1997) Cyclic GMP-dependent protein kinase and cellular signalling in the nervous system. J. Neurochem., 68, 443-456.
Woodard, C., Huang, T., Sun, H., Helfand, S.L. and Carlson, J. (1989) Genetic analysis of olfactory behavior in Drosophila: a new screen yields the ota mutants. Genetics, 123, 315-326.
Yang, M.Y., Armstrong, J.D., Vilinsky, I., Strausfeld, N.J. and Kaiser, K. (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron, 15, 45-54.
Zars, T., Fischer, M., Schulz, R. and Heisenberg, M. (2000) Localization of a short-term memory in Drosophila. Science, 288, 672-5.
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Language: | English.
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Document Type: | SYMPOSIUM: AChemS XXII Symposium.
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Journal Subset: | Clinical Medicine.
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ISSN: | 0379-864X
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NLM Journal Code: | b4b, 8217190
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