DOI: 10.1101/lm.7.1.18. Tissue-Specific Expression of a Type I Adenylyl Cyclase Rescues the <i>rutabaga</i> Mutant Memory Defect: In Search of the Engram

Tissue-Specific Expression of a Type I Adenylyl Cyclase Rescues the rutabaga Mutant Memory Defect: In Search of the Engram

10.1101/lm.7.1.18

Crossref journal-article

Cold Spring Harbor Laboratory

Learning & Memory (246)

Abstract

Most attempts to localize physical correlates of memory in the central nervous system (CNS) rely on ablation techniques. This approach has the limitation of defining just one of an unknown number of structures necessary for memory formation. We have used theDrosophila rutabaga type I Ca2+/CaM-dependent adenylyl cyclase (AC) gene to determine in which CNS region AC expression is sufficient for memory formation. Using pan-neural and restricted CNS expression with the GAL4 binary transcription activation system, we have rescued the memory defect of the rutabaga mutant in a fast robust spatial learning paradigm. The ventral ganglion, antennal lobes, and median bundle are likely the CNS structures sufficient for rutabaga AC- dependent spatial learning.

Bibliography

Zars, T., Wolf, R., Davis, R., & Heisenberg, M. (2000). Tissue-Specific Expression of a Type I Adenylyl Cyclase Rescues the rutabaga Mutant Memory Defect: In Search of the Engram. Learning & Memory, 7(1), 18â31.

Authors 4

Troy Zars (first)
Reinhard Wolf (additional)
Ron Davis (additional)
Martin Heisenberg (additional)

References 53 Referenced 124

10.1101/SQB.1983.048.01.086 / Cold Spring Harb. Symp. Quant. Biol. / Learning and memory in Drosophila, studied with mutants. by Aceves-Pina (1983)
10.1146/annurev.en.30.010185.001421
10.1101/lm.5.1.102 / Learn. & Mem. / Metamorphosis of the mushroom bodies; Large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. by Armstrong (1998)
10.3109/01677068709167218 / J. Neurogenet. / Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. by Balling (1987)
10.1523/JNEUROSCI.17-04-01493.1997 / J. Neurosci. / Experience-dependent developmental plasticity in the optic lobe of Drosophila melanogaster. by Barth (1997)
10.1242/dev.118.2.401 / Development / Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. by Brand (1993)
10.1126/science.186870
10.1126/science.274.5295.2104
10.1523/JNEUROSCI.10-02-00491.1990 / J. Neurosci. / Adaptation and fatigue of a mechanosensory neuron in wild-type Drosophila and in memory mutants. by Corfas (1990)
10.1073/pnas.88.16.7252
10.1101/lm.5.1.38 / Learn. & Mem. / Tripartite mushroom body architecture revealed by antigenic markers. by Crittenden (1998)
10.1152/physrev.1996.76.2.299 / Physiol. Rev. / Physiology and biochemistry of Drosophila learning mutants. by Davis (1996)
10.1126/science.8303280
10.1073/pnas.79.11.3646
10.1523/JNEUROSCI.16-10-03486.1996 / J. Neurosci. / Altered habituation of an identified escape circuit in Drosophila memory mutants. by Engel (1996)
10.1016/0022-1910(82)90034-8
10.1093/genetics/106.4.613 / Genetics / Conditioning mutations in Drosophila melanogaster affect an experience-dependent behavioral modification in courting males. by Gailey (1984)
10.1126/science.276.5313.795
10.1523/JNEUROSCI.15-03-01617.1995 / J. Neurosci. / Learning and memory in the honeybee. by Hammer (1995)
10.1016/0896-6273(92)90026-A
10.1007/BF00261838 / Cell Tissue Res. / Neuronal architecture of the central complex in Drosophila melanogaster. by Hanesch (1989)
10.1101/lm.5.1.1 / Learn. & Mem. / What do the mushroom bodies do for the insect brain? An introduction. by Heisenberg (1998)
10.1515/znc-1979-1-228 / Z. Naturforsch. C / Isolation of anatomical brain mutants of Drosophila melanogaster by histological means. by Heisenberg (1979)
Heisenberg M. Wolf R. (1984) Vision in Drosophila; Genetics of microbehavior. in Studies of brain function, eds Braitenberg V. Barlow H.B. Bullock T.H. Florey E. Gruesser O.-J. Peters A. (Springer-Verlag, Berlin, Germany), 12.
10.3109/01677068509100140
10.1007/s004410050901
10.1101/lm.5.1.52
10.1101/lm.6.2.177 / Learn. & Mem. / Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. by Joiner (1999)
10.1073/pnas.77.11.6912
10.1016/S0896-6273(00)80977-0
10.1016/0092-8674(92)90185-F
10.1101/gad.8.15.1787
10.1016/S0896-6273(00)80987-3
10.1016/0896-6273(95)90064-0
10.1002/cne.900880303
10.3109/01677068909066201 / J. Neurogenet. / Habituation of the landing response of Drosophila wild-type and mutants defective in olfactory learning. by Rees (1989)
Sachs L. (1992) Angewandte Statistik. (Springer-Verlag, Berlin, Germany). (10.1007/978-3-662-05747-6)
10.1073/pnas.93.12.6079
10.1016/0896-6273(93)90056-W
Strausfeld N.J. (1976) Atlas of an insect brain. (Springer-Verlag, Berlin, Germany). (10.1007/978-3-642-66179-2)
10.1007/s004270050112
10.1016/S0092-8674(00)81827-9
Wehner R. (1992) Arthropods. in Animal homing, ed Papi F. (Chapman and Hall, London, UK), pp 45–144. (10.1007/978-94-011-1588-9_3)
10.1242/jeb.199.1.125 / J. Exp. Biol. / Middle-scale navigation: The insect case. (1996)
10.1101/lm.5.1.166 / Learn. & Mem. / Drosophila mushroom bodies are dispensible for visual, tactile, and motor learning. by Wolf (1998)
10.1073/pnas.92.1.220
10.1101/lm.4.4.328
10.1007/BF00194996 / J. Comp. Physiol. [A] / A new paradigm for operant conditioning of Drosophila melanogaster. by Wustmann (1996)
10.1016/0896-6273(95)90063-2
10.1046/j.1471-4159.1994.63010041.x
10.1038/375588a0
10.1016/0896-6273(95)90309-7
10.1126/science.1670967

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 8 p.m.)
Deposited	3 years, 9 months ago (Nov. 11, 2021, 9:01 a.m.)
Indexed	1 month, 1 week ago (July 19, 2025, 11:46 p.m.)
Issued	25 years, 8 months ago (Jan. 1, 2000)
Published	25 years, 8 months ago (Jan. 1, 2000)
Published Online	25 years, 8 months ago (Jan. 1, 2000)
Published Print	25 years, 8 months ago (Jan. 1, 2000)

Funders 0

None

BibTeX

@article{Zars_2000, title={Tissue-Specific Expression of a Type I Adenylyl Cyclase Rescues the rutabaga Mutant Memory Defect: In Search of the Engram}, volume={7}, ISSN={1549-5485}, url={http://dx.doi.org/10.1101/lm.7.1.18}, DOI={10.1101/lm.7.1.18}, number={1}, journal={Learning & Memory}, publisher={Cold Spring Harbor Laboratory}, author={Zars, Troy and Wolf, Reinhard and Davis, Ron and Heisenberg, Martin}, year={2000}, month=jan, pages={18–31} }

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