Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies

Science

Volumn 274, Issue 5295, 1996, Pages 2104-2107

  Connolly, John B ^a,b   Roberts, Ian J H ^b   Armstrong, J Douglas ^c   Kaiser, Kim ^c   Forte, Michael ^d   Tully, Tim ^a   O'Kane, Cahir J ^b  

^a Simons Center for Quantitative Biology   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; DROSOPHILA; ENZYME ACTIVITY; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE INSERTION; MUSHROOM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORIMOTOR FUNCTION; STATE DEPENDENT LEARNING;

ADENYLATE CYCLASE; ANIMALS; BRAIN; CONDITIONING (PSYCHOLOGY); DROSOPHILA; ELECTROSHOCK; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; GUANOSINE TRIPHOSPHATE; NEURONS; ODORS; SIGNAL TRANSDUCTION; SMELL; TRANSGENES;

ANIMALIA; BASIDIOMYCOTA;

EID: 0030449882     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.274.5295.2104     Document Type: Article

References (44)

1. E. Kandel et al., in Synaptic Modulation and Learning: New Insights into Synaptic Transmission from the Study of Behavior (Wiley, New York, 1987), pp. 471-581; J. Byrne et al., in Advances in Second Messenger and Phosphoprotein Research, S. Shenolikar and A. Naim, Eds. (Raven, New York, 1993), pp. 47-107; E. Kandel and T. Abel, Science 268, 825 (1995).
2. E. Kandel et al., in Synaptic Modulation and Learning: New Insights into Synaptic Transmission from the Study of Behavior (Wiley, New York, 1987), pp. 471-581; J. Byrne et al., in Advances in Second Messenger and Phosphoprotein Research, S. Shenolikar and A. Naim, Eds. (Raven, New York, 1993), pp. 47-107; E. Kandel and T. Abel, Science 268, 825 (1995).
3. E. Kandel et al., in Synaptic Modulation and Learning: New Insights into Synaptic Transmission from the Study of Behavior (Wiley, New York, 1987), pp. 471-581; J. Byrne et al., in Advances in Second Messenger and Phosphoprotein Research, S. Shenolikar and A. Naim, Eds. (Raven, New York, 1993), pp. 47-107; E. Kandel and T. Abel, Science 268, 825 (1995).
4. D. Byers, R. Davis, J. Kiger, Nature 289, 79 (1981); M. Livingstone, P. Sziber, W. Quinn, Cell 37, 205 (1984); P. Drain, E. Folkers, W. Quinn, Neuron 6, 71 (1991); Z. L. Wu et al., Proc. Natl. Acad. Sci. U.S.A. 92, 220 (1995); W. Li, T. Tully, D. Kalderon, Learn. Mem, 2, 320 (1996).
5. D. Byers, R. Davis, J. Kiger, Nature 289, 79 (1981); M. Livingstone, P. Sziber, W. Quinn, Cell 37, 205 (1984); P. Drain, E. Folkers, W. Quinn, Neuron 6, 71 (1991); Z. L. Wu et al., Proc. Natl. Acad. Sci. U.S.A. 92, 220 (1995); W. Li, T. Tully, D. Kalderon, Learn. Mem, 2, 320 (1996).
6. D. Byers, R. Davis, J. Kiger, Nature 289, 79 (1981); M. Livingstone, P. Sziber, W. Quinn, Cell 37, 205 (1984); P. Drain, E. Folkers, W. Quinn, Neuron 6, 71 (1991); Z. L. Wu et al., Proc. Natl. Acad. Sci. U.S.A. 92, 220 (1995); W. Li, T. Tully, D. Kalderon, Learn. Mem, 2, 320 (1996).
7. D. Byers, R. Davis, J. Kiger, Nature 289, 79 (1981); M. Livingstone, P. Sziber, W. Quinn, Cell 37, 205 (1984); P. Drain, E. Folkers, W. Quinn, Neuron 6, 71 (1991); Z. L. Wu et al., Proc. Natl. Acad. Sci. U.S.A. 92, 220 (1995); W. Li, T. Tully, D. Kalderon, Learn. Mem, 2, 320 (1996).
8. D. Byers, R. Davis, J. Kiger, Nature 289, 79 (1981); M. Livingstone, P. Sziber, W. Quinn, Cell 37, 205 (1984); P. Drain, E. Folkers, W. Quinn, Neuron 6, 71 (1991); Z. L. Wu et al., Proc. Natl. Acad. Sci. U.S.A. 92, 220 (1995); W. Li, T. Tully, D. Kalderon, Learn. Mem, 2, 320 (1996).
9. E. Skoulakis, D. Kalderon, R. Davis, Neuron 11, 197 (1993).
10. A. Nighorn, M. Healy, R. Davis, ibid. 6, 455 (1991); P. Han, L. Levin, R. Reed, R. Davis, ibid. 9, 619 (1992).
11. A. Nighorn, M. Healy, R. Davis, ibid. 6, 455 (1991); P. Han, L. Levin, R. Reed, R. Davis, ibid. 9, 619 (1992).
12. M. Heisenberg, A. Borst, S. Wagner, D. Byers, J. Neurogenet. 2, 1 (1985); J. S. de Belle and M. Heisenberg, Proc. Natl. Acad. Sci. U.S.A. 93, 9875 (1996).
13. M. Heisenberg, A. Borst, S. Wagner, D. Byers, J. Neurogenet. 2, 1 (1985); J. S. de Belle and M. Heisenberg, Proc. Natl. Acad. Sci. U.S.A. 93, 9875 (1996).
14. J. S. de Belle and M. Heisenberg, Science 263, 692 (1994).
15. A. Brand and N. Perrimon, Development 118, 401 (1993).
16. F. Quan, W. Wolfgang, M. Forte, Proc. Natl. Acad. Sci. U.S.A. 86, 4321 (1989); W. Wolfgang et al., J. Neurosci. 10, 1014 (1990).
17. F. Quan, W. Wolfgang, M. Forte, Proc. Natl. Acad. Sci. U.S.A. 86, 4321 (1989); W. Wolfgang et al., J. Neurosci. 10, 1014 (1990).
18. F. Quan, L. Thomas, M. Forte, Proc. Natl. Acad. Sci. U.S.A. 88, 1898 (1991).
19. M. Simon, M. Strathmann, N. Gautam, Science 252, 802 (1991); H. Bourne, D. Sanders, F. McCormick, Nature 349, 117 (1991); W. Tang and A. Gilman, Cell 70, 869 (1992); A. Spiegel et al., in G Proteins (Molecular Biology Intelligence Unit, R. G. Landes Co., Austin, TX, 1994), pp. 19-20; E. Neer, Cell 60, 249 (1995).
20. M. Simon, M. Strathmann, N. Gautam, Science 252, 802 (1991); H. Bourne, D. Sanders, F. McCormick, Nature 349, 117 (1991); W. Tang and A. Gilman, Cell 70, 869 (1992); A. Spiegel et al., in G Proteins (Molecular Biology Intelligence Unit, R. G. Landes Co., Austin, TX, 1994), pp. 19-20; E. Neer, Cell 60, 249 (1995).
21. M. Simon, M. Strathmann, N. Gautam, Science 252, 802 (1991); H. Bourne, D. Sanders, F. McCormick, Nature 349, 117 (1991); W. Tang and A. Gilman, Cell 70, 869 (1992); A. Spiegel et al., in G Proteins (Molecular Biology Intelligence Unit, R. G. Landes Co., Austin, TX, 1994), pp. 19-20; E. Neer, Cell 60, 249 (1995).
22. M. Simon, M. Strathmann, N. Gautam, Science 252, 802 (1991); H. Bourne, D. Sanders, F. McCormick, Nature 349, 117 (1991); W. Tang and A. Gilman, Cell 70, 869 (1992); A. Spiegel et al., in G Proteins (Molecular Biology Intelligence Unit, R. G. Landes Co., Austin, TX, 1994), pp. 19-20; E. Neer, Cell 60, 249 (1995).
23. M. Simon, M. Strathmann, N. Gautam, Science 252, 802 (1991); H. Bourne, D. Sanders, F. McCormick, Nature 349, 117 (1991); W. Tang and A. Gilman, Cell 70, 869 (1992); A. Spiegel et al., in G Proteins (Molecular Biology Intelligence Unit, R. G. Landes Co., Austin, TX, 1994), pp. 19-20; E. Neer, Cell 60, 249 (1995).
24. sWT but lacking as a result of the Q215L mutation.
25. 238Y and 201Y are described in (7) and C232 in (18). C747 shows identical expression to that of C772 (17) (24). C309 is described by J. D. Armstrong [thesis, University of Glasgow, Scotland (1995)]. The O'Kane laboratory screened 500 P-GAL4 lines to identify OK66, OK86, OK62, OK107, OK348, and OK415.
26. T. Tully and W. Quinn, J. Comp. Physiol. 157, 263 (1985); T. Tully, T. Preat, S. Boynton, M. Del Vecchio, Cell 79, 35 (1994).
27. T. Tully and W. Quinn, J. Comp. Physiol. 157, 263 (1985); T. Tully, T. Preat, S. Boynton, M. Del Vecchio, Cell 79, 35 (1994).
28. s* insertion. We characterized a total of two P-GAL4 insertions (C232 and OK348) that expressed to some degree in the CC.
29. s* in the CC does not affect learning. Formally, however, we cannot exclude the possibility that other sites of convergence of the CS and US contribute to the conditioned behavior, as in honey-bees [M. Hammer and R. Menzel, J. Neurosci. 15, 1617 (1995)].
30. s* under UAS regulation.
31. M. Y. Yang, J. D. Armstrong, I. Vilinsky, N. Straus-field, K. Kaiser, Neuron 15, 45 (1995).
32. K. O'Dell, J. Armstrong, M. Y. Yang, K. Kaiser, ibid., p. 55.
33. Pan-neural expression was driven by P-GAL4 1407 [generated by J. Urban and G. Technau; described in L. Luo, Y. Liao, L. Jan, Y. Jan, Genes Dev. 8, 1787 (1994)].
34. s* lines. Brains from the resultant progeny were dissected, and β-Gal activity was detected as described [S. T. Sweeney, K. Broadie, J. Keane, H. Niemann, C. J. O'Kane, Neuron 14, 341 (1995)].
35. L. Levin et al., Cell 68, 479 (1992).
36. D. Cooper, N. Mons, J. Karpen, Nature 374, 421 (1995).
37. D. Clapman, Annu. Rev. Neurosci. 17, 441 (1994); W. Schreibmayer et al., Nature 380, 624 (1996).
38. D. Clapman, Annu. Rev. Neurosci. 17, 441 (1994); W. Schreibmayer et al., Nature 380, 624 (1996).
39. K. Kaiser, unpublished data.
40. S. Boynton and T. Tully, Genetics 131, 655 (1992).
41. R. Sokal and F. Rohlf, in Biometry (Freeman, New York, 1981), pp. 229-240.
42. E. Yeh, K. Gustafson, G. Boulianne, Proc. Natl. Acad. Sci. U.S.A. 92, 7036 (1995).
43. L. Luo, T. Tully, K. White, Neuron 9, 595 (1992).
44. We thank K. Moffat, J. Keane, K. Störtkuhl, R. Greenspan, M. Yang, G. Boulianne, and A. Brand for reagents. Supported by grants from the Wellcome Trust and the Science and Engineering Research Council (GR/F94989) (to C.J.O'K.), the Human Frontiers Science program (to C.J.O'K., K.K., and M.F.), and NIH grant HD 32245 (to T.T.).