Cited by 332Neurobiology and Insect Physiology ResearchMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

The DOI matches its Crossref record; 54 of the 54 references it cites were found in a registry or an index.

The amnesiac Gene Product Is Expressed in Two Neurons in the Drosophila Brain that Are Critical for Memory

Open access

Waddell, Scott, Armstrong, J.Douglas, Kitamoto, Toshihiro, Kaiser, Kim, Quinn, William G.·2000·Cell

DOI 10.1016/s0092-8674(00)00183-5

Open this paper in CoChat — free account Open PDF

Abstract

Mutations in the amnesiac gene in Drosophila affect both memory retention and ethanol sensitivity. The predicted amnesiac gene product, AMN, is an apparent preproneuropeptide, and previous studies suggest that it stimulates cAMP synthesis. Here we show that, unlike other learning-related Drosophila proteins, AMN is not preferentially expressed in mushroom bodies. Instead, it is strongly expressed in two large neurons that project over all the lobes of the mushroom bodies, a finding that suggests a modulatory role for AMN in memory formation. Genetically engineered blockade of vesicle recycling in these cells abbreviates memory as in the amnesiac mutant. Moreover, restoration of amn gene expression to these cells reestablishes normal olfactory memory in an amn deletion background. These results indicate that AMN neuropeptide release onto the mushroom bodies is critical for normal olfactory memory.

Integrity signals

Registry

Crossref · 10.1016/s0092-8674(00)00183-5

Cites

54 of 54 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Antibodies, a laboratory manual
(1989) · Biomedicine & Pharmacotherapy · doi:10.1016/0753-3322(89)90130-3 · Cited by 12,318
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes
Brand, A. H., & Perrimon, N. (1993) · Development · doi:10.1242/dev.118.2.401 · Cited by 9,510
Addiction, Dopamine, and the Molecular Mechanisms of Memory
Berke, J. D., & Hyman, S. E. (2000) · Neuron · doi:10.1016/s0896-6273(00)81056-9 · Cited by 1,184
Associative Odor Learning in Drosophila Abolished by Chemical Ablation of Mushroom Bodies
de Belle, J. S., & Heisenberg, M. (1994) · Science · doi:10.1126/science.8303280 · Cited by 797
Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic
van der Bliek, A. M., & Meyerowrtz, E. M. (1991) · Nature · doi:10.1038/351411a0 · Cited by 776
Learning and memory in the honeybee
Hammer, M., & Menzel, R. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01617.1995 · Cited by 723
Drosophila Mushroom Body Mutants are Deficient in Olfactory Learning
Heisenberg, M., Borst, A., Wagner, S., & Byers, D. (1985) · Journal of Neurogenetics · doi:10.3109/01677068509100140 · Cited by 697
Conditioned Behavior in Drosophila melanogaster
Quinn, W. G., Harris, W. A., & Benzer, S. (1974) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.71.3.708 · Cited by 695
Self-citation
An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees
Hammer, M. (1993) · Nature · doi:10.1038/366059a0 · Cited by 692
Chapter 24 Imaging Neuronal Subsets and Other Cell Types in Whole-Mount Drosophila Embryos and Larvae Using Antibody Probes
Patel, N. H. (1994) · Methods in cell biology · doi:10.1016/s0091-679x(08)60927-9 · Cited by 612

Show all 54 references

Sorted by citations

Mushroom body memoir: from maps to models
Heisenberg, M. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1074 · Cited by 1,286
The neuronal architecture of the mushroom body provides a logic for associative learning
Aso, Y., Hattori, D., Yu, Y., Johnston, R. M., Iyer, N. A., Ngo, T.-T., Dionne, H., Abbott, L., Axel, R., Tanimoto, H., et al. (2014) · eLife · doi:10.7554/elife.04577 · Cited by 1,051
Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila
Schwaerzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S., & Heisenberg, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-33-10495.2003 · Cited by 871
Conditional modification of behavior in Drosophila by targeted expression of a temperature‐sensitive shibire allele in defined neurons
Kitamoto, T. (2001) · Journal of Neurobiology · doi:10.1002/neu.1018 · Cited by 868
Self-citation
Genetic Dissection of Neural Circuits
Luo, L., Callaway, E. M., & Svoboda, K. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.002 · Cited by 771
Molecular mechanisms of memory acquisition, consolidation and retrieval
Abel, T. G., & Lattal, K. M. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00194-x · Cited by 709
Layered reward signalling through octopamine and dopamine in Drosophila
Burke, C. J., Huetteroth, W., Owald, D., Perisse, E., Krashes, M. J., Das, G., Gohl, D., Silies, M., Certel, S., & Waddell, S. (2012) · Nature · doi:10.1038/nature11614 · Cited by 614
Self-citation
OLFACTORY MEMORY FORMATION INDROSOPHILA: From Molecular to Systems Neuroscience
Davis, R. L. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135651 · Cited by 543
Drosophila neuropeptides in regulation of physiology and behavior
Nässel, D. R., & Winther, Å. M. E. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.010 · Cited by 498
Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones
Nässel, D. R. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00057-6 · Cited by 482
Neuronal assemblies of the Drosophila mushroom body
Tanaka, N. K., Tanimoto, H., & Ito, K. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21692 · Cited by 470
Drosophila: Genetics meets behaviour
Sokolowski, M. B. (2001) · Nature Reviews Genetics · doi:10.1038/35098592 · Cited by 474
The Role of Drosophila Mushroom Body Signaling in Olfactory Memory
McGuire, S. E., Le, P. T., & Davis, R. L. (2001) · Science · doi:10.1126/science.1062622 · Cited by 457
Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory
Dubnau, J., Grady, L., Kitamoto, T., & Tully, T. (2001) · Nature · doi:10.1038/35078077 · Cited by 455
Self-citation
Genetic Manipulation of Genes and Cells in the Nervous System of the Fruit Fly
Venken, K. J. T., Simpson, J. H., & Bellen, H. J. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.021 · Cited by 463
Sequential Use of Mushroom Body Neuron Subsets during Drosophila Odor Memory Processing
Krashes, M. J., Keene, A. C., Leung, B., Armstrong, J. D., & Waddell, S. (2007) · Neuron · doi:10.1016/j.neuron.2006.11.021 · Cited by 441
Self-citation
P{Switch}, a system for spatial and temporal control of gene expression in Drosophila melanogaster
Roman, G., Endo, K., Zong, L., & Davis, R. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221303998 · Cited by 406
Using translational enhancers to increase transgene expression in Drosophila
Pfeiffer, B. D., Truman, J. W., & Rubin, G. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204520109 · Cited by 397
The connectome of the adult Drosophila mushroom body provides insights into function
Li, F., Lindsey, J. W., Marin, E. C., Otto, N., Dreher, M., Dempsey, G., Stark, I., Bates, A. S., Pleijzier, M. W., Schlegel, P., et al. (2020) · eLife · doi:10.7554/elife.62576 · Cited by 418
Self-citation
The Mushroom Body of Adult Drosophila Characterized by GAL4 Drivers
Aso, Y., Grübel, K., Busch, S., Friedrich, A. B., Siwanowicz, I., & Tanimoto, H. (2009) · Journal of Neurogenetics · doi:10.1080/01677060802471718 · Cited by 381
Drosophila olfactory memory: single genes to complex neural circuits
Keene, A. C., & Waddell, S. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2098 · Cited by 384
Self-citation
A connectome of a learning and memory center in the adult Drosophila brain
Takemura, S.-Y., Aso, Y., Hige, T., Wong, A., Lu, Z., Xu, C. S., Rivlin, P. K., Hess, H., Zhao, T., Parag, T., et al. (2017) · eLife · doi:10.7554/elife.26975 · Cited by 367
Deconstructing Memory in Drosophila
Margulies, C. E., Tully, T., & Dubnau, J. (2005) · Current Biology · doi:10.1016/j.cub.2005.08.024 · Cited by 336
STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN
Fahrbach, S. E. (2005) · Annual Review of Entomology · doi:10.1146/annurev.ento.51.110104.150954 · Cited by 318
A genetically encoded sensor for measuring serotonin dynamics
Wan, J., Peng, W., Li, X., Qian, T., Song, K., Zeng, J., Deng, F., Hao, S., Feng, J., Zhang, P., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00823-7 · Cited by 302
Rapid Consolidation to aradishand Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning inDrosophila
Krashes, M. J., & Waddell, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5333-07.2008 · Cited by 297
Self-citation
Dopamine Is Required for Learning and Forgetting in Drosophila
Berry, J. A., Cervantes-Sandoval, I., Nicholas, E. P., & Davis, R. L. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.007 · Cited by 311
Traces of Drosophila Memory
Davis, R. L. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.012 · Cited by 300
Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila
Cognigni, P., Felsenberg, J., & Waddell, S. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.12.002 · Cited by 281
Self-citation
Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster
Eckstein, N., Bates, A. S., Champion, A., Du, M., Yin, Y., Schlegel, P., Lu, A. K.-Y., Rymer, T., Finley-May, S., Paterson, T., et al. (2024) · Cell · doi:10.1016/j.cell.2024.03.016 · Cited by 277
“…morphology—in which co-transmission is known to occur, e.g. , Kenyon cells (acetylcholine/sNPF/others) (Croset et al., 2018), DPM (GABA/serotonin/amnesiac) (Waddell et al., 2000), Mi15 (acetylcholine/serotonin) (Davis et al., 2020) and PPL101-6 DANs (dopamine/serotonin) (Mao and Davis, 2009).”
Neuropeptides as Regulators of Behavior in Insects
Schoofs, L., LOOF, A. D., & Hiel, M. B. V. (2016) · Annual Review of Entomology · doi:10.1146/annurev-ento-031616-035500 · Cited by 269
Ras Activity in the Drosophila Prothoracic Gland Regulates Body Size and Developmental Rate via Ecdysone Release
Caldwell, P. E., Walkiewicz, M. A., & Stern, M. (2005) · Current Biology · doi:10.1016/j.cub.2005.09.011 · Cited by 274
Drosophila α/β Mushroom Body Neurons Form a Branch-Specific, Long-Term Cellular Memory Trace after Spaced Olfactory Conditioning
Yu, D., Akalal, D.-B. G., & Davis, R. L. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.030 · Cited by 266
Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP
Wang, H., Ferguson, G. D., Pineda, V. V., Cundiff, P. E., & Storm, D. R. (2004) · Nature Neuroscience · doi:10.1038/nn1248 · Cited by 244
NMDA Receptors Mediate Olfactory Learning and Memory in Drosophila
Xia, S., Miyashita, T., Fu, T., Lin, W., Wu, C., Pyzocha, L., Lin, I.-R., Saitoe, M., Tully, T., & Chiang, A. (2005) · Current Biology · doi:10.1016/j.cub.2005.02.059 · Cited by 231
A Map of Olfactory Representation in the Drosophila Mushroom Body
Lin, H., Lai, J. S.-Y., Chin, A., Chen, Y., & Chiang, A. (2007) · Cell · doi:10.1016/j.cell.2007.03.006 · Cited by 224
Altered Representation of the Spatial Code for Odors after Olfactory Classical Conditioning
Yu, D., Ponomarev, A. L., & Davis, R. L. (2004) · Neuron · doi:10.1016/s0896-6273(04)00217-x · Cited by 222
Thirty years of olfactory learning and memory research in Drosophila melanogaster
McGuire, S. E., Deshazer, M., & Davis, R. L. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.09.003 · Cited by 220
Dynamics of Learning-Related cAMP Signaling and Stimulus Integration in the Drosophila Olfactory Pathway
Tomchik, S. M., & Davis, R. L. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.029 · Cited by 217
Invertebrate models of drug abuse
Wolf, F. W., & Heberlein, U. (2002) · Journal of Neurobiology · doi:10.1002/neu.10166 · Cited by 216
Chapter 3 Neurogenetics of Courtship and Mating in Drosophila
Villella, A., & Hall, J. C. (2008) · Advances in genetics · doi:10.1016/s0065-2660(08)00603-2 · Cited by 209
Neuropeptides in interneurons of the insect brain
Nässel, D. R., & Homberg, U. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0210-8 · Cited by 208
Activation of Trk Neurotrophin Receptor Signaling by Pituitary Adenylate Cyclase-activating Polypeptides
Lee, F. S., Rajagopal, R., Kim, A. H., Chang, P. C.-Y., & Chao, M. V. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m107421200 · Cited by 200
TrpA1 Regulates Thermal Nociception in Drosophila
Neely, G. G., Keene, A. C., Duchek, P., Chang, E. C., Wang, Q., Aksoy, Y. A., Rosenzweig, M. R., Costigan, M., Woolf, C. J., Garrity, P., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024343 · Cited by 191
Drosophilaas a new model organism for the neurobiology of aggression?
Baier, A., Wittek, B., & Brembs, B. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.205.9.1233 · Cited by 187
A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster
Haynes, P. R., Christmann, B. L., & Griffith, L. C. (2015) · eLife · doi:10.7554/elife.03868 · Cited by 186
Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression
Blanchardon, E., Grima, B., Klarsfeld, A., Chélot, E., Hardin, P. E., Préat, T., & Rouyer, F. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2000.01450.x · Cited by 179
Flies, Genes, and Learning
Waddell, S., & Quinn, W. G. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1283 · Cited by 184
Self-citation
Extinction Antagonizes Olfactory Memory at the Subcellular Level
Schwärzel, M., Heisenberg, M., & Zars, T. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)00832-2 · Cited by 187
An engram found? Evaluating the evidence from fruit flies
Gerber, B., Tanimoto, H., & Heisenberg, M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.10.014 · Cited by 181
HEN-1, a Secretory Protein with an LDL Receptor Motif, Regulates Sensory Integration and Learning in Caenorhabditis elegans
Ishihara, T., Iino, Y., Mohri, A., Mori, I., Gengyo‐Ando, K., Mitani, S., & Katsura, I. (2002) · Cell · doi:10.1016/s0092-8674(02)00748-1 · Cited by 181
Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body
Wu, C., Xia, S., Fu, T., Wang, H., Chen, Y.-H., Leong, D. J., Chiang, A., & Tully, T. (2007) · Nature Neuroscience · doi:10.1038/nn2005 · Cited by 180
Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila
Yamaguchi, S., Desplan, C., & Heisenberg, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809398107 · Cited by 171
Aging Specifically Impairs amnesiac-Dependent Memory in Drosophila
Tamura, T., Chiang, A., Ito, N., Liu, H., Horiuchi, J., Tully, T., & Saitoe, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00732-3 · Cited by 171
Drosophila DPM Neurons Form a Delayed and Branch-Specific Memory Trace after Olfactory Classical Conditioning
Yu, D., Keene, A. C., Srivatsan, A., Waddell, S., & Davis, R. L. (2005) · Cell · doi:10.1016/j.cell.2005.09.037 · Cited by 167
Self-citation
Functional neuroanatomy of Drosophila olfactory memory formationPreprint
Guven-Ozkan, T., & Davis, R. L. (2014) · Learning & Memory · doi:10.1101/lm.034363.114 · Cited by 177
Learning and Memory in Drosophila: Behavior, Genetics, and Neural Systems
Kahsai, L., & Zars, T. D. (2011) · International review of neurobiology · doi:10.1016/b978-0-12-387003-2.00006-9 · Cited by 163
The mushroom bodies of Drosophila melanogaster: An immunocytological and golgi study of Kenyon cell organization in the calyces and lobes
Strausfeld, N. J., Sinakevitch, I. G., & Vilinsky, I. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10368 · Cited by 155
Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch
Mao, Z., Roman, G., Zong, L., & Davis, R. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306128101 · Cited by 153
Retrograde Signaling by Syt 4 Induces Presynaptic Release and Synapse-Specific Growth
Yoshihara, M., Adolfsen, B., Galle, K. T., & Littleton, J. T. (2005) · Science · doi:10.1126/science.1117541 · Cited by 153
Neuronal wiring diagram of an adult brain
Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Lin, A., Costa, M., Eichler, K., Yin, Y., et al. (2023) · doi:10.1101/2023.06.27.546656 · Cited by 149
Diverse Odor-Conditioned Memories Require Uniquely Timed Dorsal Paired Medial Neuron Output
Keene, A. C., Stratmann, M., Keller, A., Perrat, P. N., Vosshall, L. B., & Waddell, S. (2004) · Neuron · doi:10.1016/j.neuron.2004.10.006 · Cited by 149
Self-citation
Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila
Lee, P.-T., Lin, H.-W., Chang, Y. A., Fu, T., Dubnau, J., Hirsh, J., Lee, T., & Chiang, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019483108 · Cited by 147
Evolution of insect mushroom bodies: old clues, new insights
Farris, S. M. (2005) · Arthropod Structure & Development · doi:10.1016/j.asd.2005.01.008 · Cited by 146
Functional architecture of reward learning in mushroom body extrinsic neurons of larval Drosophila
Saumweber, T., Rohwedder, A., Schleyer, M. H., Eichler, K., Chen, Y., Aso, Y., Cardona, A., Eschbach, C., Kobler, O., Voigt, A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03130-1 · Cited by 154
Roles for Drosophila mushroom body neurons in olfactory learning and memoryPreprint
Akalal, D.-B. G., Wilson, C. F., Zong, L., Tanaka, N. K., Ito, K., & Davis, R. L. (2006) · Learning & Memory · doi:10.1101/lm.221206 · Cited by 138
Drosophila Dorsal Paired Medial Neurons Provide a General Mechanism for Memory Consolidation
Keene, A. C., Krashes, M. J., Leung, B., Bernard, J. A., & Waddell, S. (2006) · Current Biology · doi:10.1016/j.cub.2006.06.022 · Cited by 137
Self-citation
A Pair of Inhibitory Neurons Are Required to Sustain Labile Memory in the Drosophila Mushroom Body
Pitman, J. L., Huetteroth, W., Burke, C. J., Krashes, M. J., Lai, S.-L., Lee, T., & Waddell, S. (2011) · Current Biology · doi:10.1016/j.cub.2011.03.069 · Cited by 137
Self-citation
Molecular biology and anatomy of Drosophila olfactory associative learning
Roman, G., & Davis, R. L. (2001) · BioEssays · doi:10.1002/bies.1083 · Cited by 134
Pokes, sunburn, and hot sauce: Drosophila as an emerging model for the biology of nociception
Im, S. H., & Galko, M. J. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22737 · Cited by 135
Network statistics of the whole-brain connectome of Drosophila
Lin, A., Yang, R., Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Costa, M., Eichler, K., et al. (2024) · Nature · doi:10.1038/s41586-024-07968-y · Cited by 147
Drosophila fasciclinII Is Required for the Formation of Odor Memories and for Normal Sensitivity to Alcohol
Cheng, Y., Endo, K., Wu, K., Rodan, A. R., Heberlein, U., & Davis, R. L. (2001) · Cell · doi:10.1016/s0092-8674(01)00386-5 · Cited by 129
Multimodal sensory integration in insects—towards insect brain control architectures
Wessnitzer, J., & Webb, B. H. (2006) · Bioinspiration & Biomimetics · doi:10.1088/1748-3182/1/3/001 · Cited by 127
Multiple Amidated Neuropeptides Are Required for Normal Circadian Locomotor Rhythms inDrosophila
Taghert, P. H., Hewes, R. S., Park, J. H., O’Brien, M. A., Han, M., & Peck, M. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06673.2001 · Cited by 126
Imaging of an Early Memory Trace in theDrosophilaMushroom Body
Wang, Y., Mamiya, A., Chiang, A., & Zhong, Y. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2958-07.2008 · Cited by 124
Olfaction and olfactory learning in Drosophila: recent progress
Fiala, A. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.11.009 · Cited by 124
Centrophobism/thigmotaxis, a new role for the mushroom bodies inDrosophila
Besson, M., & Martin, J.-R. (2004) · Journal of Neurobiology · doi:10.1002/neu.20111 · Cited by 121
An Octopamine-Mushroom Body Circuit Modulates the Formation of Anesthesia-Resistant Memory in Drosophila
Wu, C., Shih, M.-F. M., Lee, P.-T., & Chiang, A. (2013) · Current Biology · doi:10.1016/j.cub.2013.09.056 · Cited by 118
Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: Relations to extrinsic neurons expressing different neurotransmitters
Johard, H. A. D., Enell, L. E., Gustafsson, E., Trifilieff, P., Veenstra, J. A., & Nässel, D. R. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21636 · Cited by 120
Conditional disruption of synaptic transmission induces male–male courtship behavior in Drosophila
Kitamoto, T. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202489099 · Cited by 120
Self-citation
Neural substrates of memory: From synapse to system
Dubnau, J., Chiang, A., & Tully, T. (2002) · Journal of Neurobiology · doi:10.1002/neu.10170 · Cited by 118
Neurotransmitter Classification from Electron Microscopy Images at Synaptic Sites in Drosophila Melanogaster
Eckstein, N., Bates, A. S., Champion, A., Du, M., Yin, Y., Schlegel, P., Lu, A. K.-Y., Rymer, T., Finley-May, S., Paterson, T., et al. (2020) · doi:10.1101/2020.06.12.148775 · Cited by 115
Heterotypic Gap Junctions between Two Neurons in the Drosophila Brain Are Critical for Memory
Wu, C., Shih, M.-F. M., Lai, J. S.-Y., Yang, H.-T., Turner, G. C., Chen, L., & Chiang, A. (2011) · Current Biology · doi:10.1016/j.cub.2011.02.041 · Cited by 112
Smelling, Tasting, Learning: Drosophila as a Study Case
Gerber, B., Stocker, R. F., Tanimura, T., & Thum, A. S. (2009) · Results and problems in cell differentiation · doi:10.1007/400_2008_9 · Cited by 112
Hmgcr in the Corpus Allatum Controls Sexual Dimorphism of Locomotor Activity and Body Size via the Insulin Pathway in Drosophila
Belgacem, Y. H., & Martin, J. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000187 · Cited by 110
Distinctive Neuronal Networks and Biochemical Pathways for Appetitive and Aversive Memory inDrosophilaLarvae
Honjo, K., & Furukubo-Tokunaga, K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1315-08.2009 · Cited by 106
Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies
Jefferis, G. S. X. E., Marin, E. C., Watts, R. J., & Luo, L. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00293-3 · Cited by 106
Sequential Learning of Pheromonal Cues Modulates Memory Consolidation in Trainer-Specific Associative Courtship Conditioning
Ejima, A., Smith, B. P. C., Lucas, C., Levine, J. D., & Griffith, L. C. (2005) · Current Biology · doi:10.1016/j.cub.2005.01.035 · Cited by 105
The Receptor Tyrosine Kinase Alk Controls Neurofibromin Functions in Drosophila Growth and Learning
Gouzi, J. Y., Moressis, A., Walker, J. A., Apostolopoulou, A. A., Palmer, R. H., Bernards, A., & Skoulakis, E. M. C. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002281 · Cited by 103
Drosophila Larvae Establish Appetitive Olfactory Memories via Mushroom Body Neurons of Embryonic Origin
Pauls, D., Selcho, M., Gendre, N., Stocker, R. F., & Thum, A. S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1281-10.2010 · Cited by 103
Chapter 3 Mapping and Manipulating Neural Circuits in the Fly Brain
Simpson, J. H. (2009) · Advances in genetics · doi:10.1016/s0065-2660(09)65003-3 · Cited by 105
Operant conditioning in invertebrates
Brembs, B. (2003) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2003.10.002 · Cited by 102
Drosophila Neuropeptide Signaling
Taghert, P. H., & Veenstra, J. A. (2003) · Advances in genetics · doi:10.1016/s0065-2660(03)01001-0 · Cited by 97
System-Like Consolidation of Olfactory Memories in Drosophila
Cervantes-Sandoval, I., Martín‐Peña, A., Berry, J. A., & Davis, R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0451-13.2013 · Cited by 96
Of Flies and Man:Drosophilaas a Model for Human Complex Traits
Mackay, T. F. C., & Anholt, R. R. H. (2006) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.7.080505.115758 · Cited by 96
What can we teach Drosophila? What can they teach us?
Waddell, S., & Quinn, W. G. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02526-4 · Cited by 92
Self-citation
Presynapses in Kenyon Cell Dendrites in the Mushroom Body Calyx of Drosophila
Christiansen, F., Zube, C., Andlauer, T. F. M., Wichmann, C., Fouquet, W., Owald, D., Mertel, S., Leiss, F., Tavosanis, G., Luna, A. J. F., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6542-10.2011 · Cited by 90
Sleep in Insects
Helfrich‐Förster, C. (2017) · Annual Review of Entomology · doi:10.1146/annurev-ento-020117-043201 · Cited by 89
Functional Dissection of Neuroanatomical Loci Regulating Ethanol Sensitivity inDrosophila
Rodan, A. R., Kiger, J. A., & Heberlein, U. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-21-09490.2002 · Cited by 89
The Serotonergic Central Nervous System of the Drosophila Larva: Anatomy and Behavioral Function
Huser, A., Rohwedder, A., Apostolopoulou, A. A., Widmann, A., Pfitzenmaier, J. E., Maiolo, E. M., Selcho, M., Pauls, D., von Essen, A. M. H. J., Gupta, T., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047518 · Cited by 95

Authors: Waddell, S., Armstrong, J. D., Kitamoto, T., Kaiser, K., & Quinn, W. G.
Affiliations: Massachusetts Institute of Technology (US)
University of Glasgow (GB)
Beckman Research Institute (US)
Corresponding author: Waddell, Scott
ORCID: Waddell, Scott
Armstrong, J.Douglas
Kitamoto, Toshihiro
Quinn, William G.
Venue: Cell
Publisher: Elsevier BV
Published: 2000-11
Volume: 103
Issue: 5
Pages: 805-813
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/s0092-8674(00)00183-5
OpenAlex: W2140882620
Cited by: 332
References: 54
Citations by year: 2026: 8 · 2025: 12 · 2024: 12 · 2023: 13 · 2022: 7 · 2021: 7 · 2020: 9 · 2019: 5 · 2018: 13 · 2017: 14 · 2016: 8 · 2015: 13 · 2014: 7 · 2013: 14 · 2012: 12
FWCI: 6.65
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 4641 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: olfactory memory, mushroom body, vesicle recycling, neuropeptide release, memory retention, ethanol sensitivity, cAMP signaling, memory formation
MeSH terms: Cyclic AMP, Animals, Brain, Chromosomes, Drosophila, Genotype, Immunohistochemistry, Memory, Models, Biological, Mutation, Neurons, Neuropeptides, Peptides, Phenotype, Smell, Temperature, Time Factors, Gene Deletion, Genes, Reporter, Drosophila Proteins, Animals, Genetically Modified

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The amnesiac Gene Product Is Expressed in Two Neurons in the Drosophila Brain that Are Critical for Memory

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks