A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila
Open accessAbstract
Behavioral expression of food-associated memory in fruit flies is constrained by satiety and promoted by hunger, suggesting an influence of motivational state. Here, we identify a neural mechanism that integrates the internal state of hunger and appetitive memory. We show that stimulation of neurons that express neuropeptide F (dNPF), an ortholog of mammalian NPY, mimics food deprivation and promotes memory performance in satiated flies. Robust appetitive memory performance requires the dNPF receptor in six dopaminergic neurons that innervate a distinct region of the mushroom bodies. Blocking these dopaminergic neurons releases memory performance in satiated flies, whereas stimulation suppresses memory performance in hungry flies. Therefore, dNPF and dopamine provide a motivational switch in the mushroom body that controls the output of appetitive memory.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
In insects, small populations of aminergic cells signal aspects of the state of the insect and provide reinforcement signals to the learning and memory centres of the mushroom bodies, so that the subjective meaning of objects in the environment to the organism can be learnt.
“In insects, small populations of aminergic cells signal aspects of the state of the insect and also provide reinforcement signals to the learning and memory centres of the mushroom bodies [69,70], so that the subjective meaning of objects in the environment to the organism can be learnt [70–72].”
From Phenomenal interface theory: a model for basal consciousness (2025) · cites this paper as [69]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Handbook of brain theory and neural networks
(1996) · Choice Reviews Online · doi:10.5860/choice.33-4484 · Cited by 3,913 · see citing works
Identification of a cold receptor reveals a general role for TRP channels in thermosensation
McKemy, D. D., Neuhausser, W., & Julius, D. J. (2002) · Nature · doi:10.1038/nature719 · Cited by 2,716 · see citing works
A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila
Dietzl, G., Chen, D., Schnorrer, F., Su, K.-C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., et al. (2007) · Nature · doi:10.1038/nature05954 · Cited by 2,644 · see citing works
Lee, T., & Luo, L. (1999) · Neuron · doi:10.1016/s0896-6273(00)80701-1 · Cited by 2,540 · see citing works
Purposive Behavior in Animals and Men
Rodhom, C., & Tolman, E. C. (1950) · The American Journal of Psychology · doi:10.2307/1418946 · Cited by 2,455 · see citing works
A TRP Channel that Senses Cold Stimuli and Menthol
Peier, A. M., Moqrich, A., Hergarden, A. C., Reeve, A. J., Andersson, D. A., Story, G. M., Earley, T. J., Dragoni, I., McIntyre, P., Bevan, S., et al. (2002) · Cell · doi:10.1016/s0092-8674(02)00652-9 · Cited by 2,361 · see citing works
Tatemoto, K., Carlquist, M., & Mutt, V. (1982) · Nature · doi:10.1038/296659a0 · Cited by 2,254 · see citing works
Purposive Behavior in Animals and Men
Irwin, F. W. (1932) · Europe PMC (PubMed Central) · Cited by 1,867 · see citing works
Learning and Instinct in Animals
Kennedy, J. S., & Thorpe, W. H. (1964) · Journal of Animal Ecology · doi:10.2307/2644 · Cited by 1,598 · see citing works
The Handbook of brain theory and neural networks
(2003) · Choice Reviews Online · doi:10.5860/choice.41-0300 · Cited by 1,540 · see citing works
NEUROPEPTIDE Y AND HUMAN PANCREATIC POLYPEPTIDE STIMULATE FEEDING BEHAVIOR IN RATS
Clark, J. T., Kalra, P. S., Crowley, W. R., & Kalra, S. P. (1984) · Endocrinology · doi:10.1210/endo-115-1-427 · Cited by 1,276 · see citing works
Classical conditioning and retention in normal and mutantDrosophila melanogaster
Tully, T., & Quinn, W. G. (1985) · Journal of Comparative Physiology A · doi:10.1007/bf01350033 · Cited by 1,189 · see citing works
NPY/AgRP Neurons Are Essential for Feeding in Adult Mice but Can Be Ablated in Neonates
Luquet, S. H., Perez, F. A., Hnasko, T. S., & Palmiter, R. D. (2005) · Science · doi:10.1126/science.1115524 · Cited by 1,127 · see citing works
Saper, C. B., Chou, T. C., & Elmquist, J. K. (2002) · Neuron · doi:10.1016/s0896-6273(02)00969-8 · Cited by 1,120 · see citing works
An internal thermal sensor controlling temperature preference in Drosophila
Hamada, F. N., Rosenzweig, M. R., Kang, K., Pulver, S. R., Ghezzi, A., Jegla, T. J., & Garrity, P. (2008) · Nature · doi:10.1038/nature07001 · Cited by 1,076 · see citing works
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 · see citing works
Kitamoto, T. (2001) · Journal of Neurobiology · doi:10.1002/neu.1018 · Cited by 868 · see citing works
The BDGP Gene Disruption Project
Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans-Holm, M. E., Hiesinger, P. R., Schulze, K. L., Rubin, G. M., et al. (2004) · Genetics · doi:10.1534/genetics.104.026427 · Cited by 864 · see citing works
Animal Behaviour: A Synthesis of Ethology and Comparative Psychology
Cullen, J. M., & Hinde, R. A. (1968) · Journal of Animal Ecology · doi:10.2307/3093 · Cited by 846 · see citing works
Agouti-related peptide–expressing neurons are mandatory for feeding
Gropp, E., Shanabrough, M., Borók, E., Xu, A. W., Janoschek, R., Buch, T., Plum, L., Balthasar, N., Hampel, B., Waisman, A., et al. (2005) · Nature Neuroscience · doi:10.1038/nn1548 · Cited by 800 · see citing works
Stanley, B. G., & LEIBOWITZ, S. F. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.11.3940 · Cited by 741 · see citing works
Learning and instinct in animals
Brown, D. R. (1957) · Journal of the Franklin Institute · doi:10.1016/0016-0032(57)90298-3 · Cited by 685 · see citing works
Localization of a Short-Term Memory in Drosophila
Zars, T. D., Fischer, M., Schulz, R. A., & Heisenberg, M. (2000) · Science · doi:10.1126/science.288.5466.672 · Cited by 600 · see citing works
Dopamine Is a Regulator of Arousal in the Fruit Fly
Kume, K., Kume, S., Park, S. K., Hirsh, J., & Jackson, F. R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2048-05.2005 · Cited by 597 · see citing works
Animal Behavior: A Synthesis of Ethology and Comparative Psychology
Stokes, A. W., & Hinde, R. A. (1967) · Journal of Wildlife Management · doi:10.2307/3798339 · Cited by 596 · see citing works
Schroll, C., Riemensperger, T. D., Bucher, D. B., Ehmer, J., Völler, T., Erbguth, K., Gerber, B., Hendel, T., Nagel, G., Buchner, E., et al. (2006) · Current Biology · doi:10.1016/j.cub.2006.07.023 · Cited by 587 · see citing works
Friggi‐Grelin, F., Coulom, H., Meller, M., Gomez, D., Hirsh, J., & Birman, S. (2003) · Journal of Neurobiology · doi:10.1002/neu.10185 · Cited by 561 · see citing works
Mao, Z. (2009) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.005.2009 · Cited by 532 · see citing works
Sahu, A., Kalra, P. S., & Kalra, S. P. (1988) · Peptides · doi:10.1016/0196-9781(88)90013-7 · Cited by 503 · see citing works
Associative Learning Disrupted by Impaired G s Signaling in Drosophila Mushroom Bodies
Connolly, J. B., Roberts, I. J. H., Armstrong, J. D., Kaiser, K., Forte, M. A., Tully, T., & O’Kane, C. J. (1996) · Science · doi:10.1126/science.274.5295.2104 · Cited by 490 · see citing works
Self-citationNeuronal assemblies of the <i>Drosophila</i> mushroom body
Tanaka, N. K., Tanimoto, H., & Ito, K. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21692 · Cited by 470 · see citing works
Sleep in Drosophila is regulated by adult mushroom bodies
Joiner, W. J., Crocker, A. J., White, B. H., & Sehgal, A. (2006) · Nature · doi:10.1038/nature04811 · Cited by 455 · see citing works
Self-citationThe staufen/pumilio Pathway Is Involved in Drosophila Long-Term Memory
Dubnau, J., Chiang, A., Grady, L., Barditch, J., Gossweiler, S., McNeil, J., Smith, P., Buldoc, F., Scott, R., Certa, U., et al. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00064-2 · Cited by 449 · see citing works
The D <sub>2</sub> Dopamine Receptor Gene as a Determinant of Reward Deficiency Syndrome
Blum, K., Sheridan, P. J., Wood, R. C., Braverman, E. R., Chen, T. J. H., phd, J. G. C., & Comings, D. E. (1996) · Journal of the Royal Society of Medicine · doi:10.1177/014107689608900711 · Cited by 443 · see citing works
Developmental Control of Foraging and Social Behavior by the Drosophila Neuropeptide Y-like System
Wu, Q., Wen, T., Lee, G., Park, J. H., Cai, H. N., & Shen, P. (2003) · Neuron · doi:10.1016/s0896-6273(03)00396-9 · Cited by 432 · see citing works
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 422 · see citing works
Self-citationDistinct memory traces for two visual features in the Drosophila brain
Liu, G., Seiler, H., Wen, A., Zars, T. D., Ito, K., Wolf, R., Heisenberg, M., & Liu, L. (2006) · Nature · doi:10.1038/nature04381 · Cited by 407 · see citing works
Neuropeptide Y Stimulates Feeding but Inhibits Sexual Behavior in Rats*
Clark, J. T., Kalra, P. S., & Kalra, S. P. (1985) · Endocrinology · doi:10.1210/endo-117-6-2435 · Cited by 392 · see citing works
Reward learning in normal and mutant Drosophila
Tempel, B. L., Bonini, N. M., Dawson, D. R., & Quinn, W. G. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.5.1482 · Cited by 391 · see citing works
CARPENTER, M. B. (1968) · Neurology · doi:10.1212/wnl.18.3.316 · Cited by 385 · see citing works
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 · see citing works
Self-citationLeeper, R. R., & Hull, C. L. (1952) · The American Journal of Psychology · doi:10.2307/1418777 · Cited by 375 · see citing works
Localization of Long-Term Memory Within the Drosophila Mushroom Body
Pascual, A., & Préat, T. (2001) · Science · doi:10.1126/science.1064200 · Cited by 368 · see citing works
Kim, Y.-C., Lee, H.-G., & Han, K. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1167-07.2007 · Cited by 365 · see citing works
Excitatory Local Circuits and Their Implications for Olfactory Processing in the Fly Antennal Lobe
Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M., & Miesenböck, G. (2007) · Cell · doi:10.1016/j.cell.2006.12.034 · Cited by 359 · see citing works
Dopaminergic Modulation of Arousal in Drosophila
Waldowski, R. A., van Swinderen, B., & Greenspan, R. J. (2005) · Current Biology · doi:10.1016/j.cub.2005.05.025 · Cited by 359 · see citing works
Punishment Prediction by Dopaminergic Neurons in Drosophila
Riemensperger, T. D., Völler, T., Stock, P., Buchner, E., & Fiala, A. (2005) · Current Biology · doi:10.1016/j.cub.2005.09.042 · Cited by 350 · see citing works
A dynamic role for the mushroom bodies in promoting sleep in Drosophila
Pitman, J. L., McGill, J. J., Keegan, K. P., & Allada, R. (2006) · Nature · doi:10.1038/nature04739 · Cited by 330 · see citing works
Sanacora, G., Kershaw, M., Finkelstein, J. A., & White, J. D. (1990) · Endocrinology · doi:10.1210/endo-127-2-730 · Cited by 309 · see citing works
Krashes, M. J., & Waddell, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5333-07.2008 · Cited by 297 · see citing works
Self-citationSerotonin is necessary for place memory in Drosophila
Sitaraman, D., Zars, M., LaFerriere, H., Chen, Y.-C., Sable-Smith, A., Kitamoto, T., Rottinghaus, G. E., & Zars, T. D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710168105 · Cited by 291 · see citing works
NPY and Y receptors: lessons from transgenic and knockout models
Lin, S., Boey, D., & Herzog, H. (2004) · Neuropeptides · doi:10.1016/j.npep.2004.05.005 · Cited by 282 · see citing works
Regulation of aversion to noxious food by Drosophila neuropeptide Y– and insulin-like systems
Wu, Q., Zhao, Z., & Shen, P. (2005) · Nature Neuroscience · doi:10.1038/nn1540 · Cited by 279 · see citing works
Candidate Gustatory Interneurons Modulating Feeding Behavior in the Drosophila Brain
Melcher, C., & Pankratz, M. J. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030305 · Cited by 278 · see citing works
The Drosophila takeout Gene Is a Novel Molecular Link between Circadian Rhythms and Feeding Behavior
Sarov‐Blat, L., So, W. V., Liu, L., & Rosbash, M. (2000) · Cell · doi:10.1016/s0092-8674(00)80876-4 · Cited by 271 · see citing works
Yu, D., Akalal, D.-B. G., & Davis, R. L. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.030 · Cited by 266 · see citing works
Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family
Brown, M. R., CRIM, J. W., Arata, R. C., et al. (1999) · Peptides · doi:10.1016/s0196-9781(99)00097-2 · Cited by 257 · see citing works
Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila
Wu, Q., Zhang, Y., Xu, J., & Shen, P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501914102 · Cited by 254 · see citing works
Postembryonic ablation of AgRP neurons in mice leads to a lean, hypophagic phenotype
Bewick, G. A., Gardiner, J., Dhillo, W. S., Kent, A. S., White, N. E., Webster, Z., Ghatei, M. A., & Bloom, S. R. (2005) · The FASEB Journal · doi:10.1096/fj.04-3434fje · Cited by 235 · see citing works
Mushroom Bodies Suppress Locomotor Activity in Drosophila melanogasterPreprint
Martin, J.-R., Ernst, R., & Heisenberg, M. (1998) · Learning & Memory · doi:10.1101/lm.5.1.179 · Cited by 227 · see citing works
Neuropeptide Y action in the rat hippocampal slice: site and mechanism of presynaptic inhibition
Colmers, W., Lukowiak, K. D., & Pittman, Q. J. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-10-03827.1988 · Cited by 222 · see citing works
Qian, J., Colmers, W. F., & Saggau, P. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08169.1997 · Cited by 210 · see citing works
Dopamine-Mushroom Body Circuit Regulates Saliency-Based Decision-Making in Drosophila
Zhang, K., Guo, J., Peng, Y., Xi, W., & Guo, A. (2007) · Science · doi:10.1126/science.1137357 · Cited by 203 · see citing works
Insulin, leptin, and food reward: update 2008
Figlewicz, D. P., & Benoit, S. C. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90725.2008 · Cited by 202 · see citing works
Wen, T., Parrish, C. A., Xu, D., Wu, Q., & Shen, P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406814102 · Cited by 197 · see citing works
Animal Behaviour–A Synthesis of Ethology and Comparative Psychology.
Secord, A. C. (1967) · Europe PMC (PubMed Central) · Cited by 191 · see citing works
Colmers, W. F., Klapstein, G. J., Fournier, A., St-Pierre, S. A., & Treherne, K. A. (1991) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1991.tb12129.x · Cited by 189 · see citing works
Dopamine and impulse control disorders in Parkinson's disease
Weintraub, D. A. (2009) · Annals of Neurology · doi:10.1002/ana.21454 · Cited by 189 · see citing works
Seugnet, L., Suzuki, Y., Vine, L., Gottschalk, L., & Shaw, P. J. (2008) · Current Biology · doi:10.1016/j.cub.2008.07.028 · Cited by 188 · see citing works
Brain circuits regulating energy homeostasis
Abizaid, A. B., & Horváth, T. L. (2008) · Regulatory Peptides · doi:10.1016/j.regpep.2007.10.006 · Cited by 171 · see citing works
Characterization of a functional neuropeptide F receptor from Drosophila melanogaster
Garczynski, S. F., Brown, M. R., Shen, P., et al. (2002) · Peptides · doi:10.1016/s0196-9781(01)00647-7 · Cited by 167 · see citing works
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 · see citing works
Self-citationRegulation of feeding behaviour and locomotor activity bytakeoutinDrosophila
Meunier, N., Belgacem, Y. H., & Martin, J. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.02755 · Cited by 157 · see citing works
Arquier, N., Géminard, C., Bourouis, M., et al. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.02.003 · Cited by 138 · see citing works
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 · see citing works
Self-citationOn the sites of presynaptic inhibition by neuropeptide y in rat hippocampus in vitro
Klapstein, G. J., & Colmers, W. F. (1993) · Hippocampus · doi:10.1002/hipo.450030111 · Cited by 134 · see citing works
Perspectives in Chemoreception and Behavior
(1987) · Proceedings in life sciences · doi:10.1007/978-1-4612-4644-2 · Cited by 131 · see citing works
Kim, Y.-C., Lee, H.-G., Seong, C.-S., & Han, K. (2003) · Gene Expression Patterns · doi:10.1016/s1567-133x(02)00098-4 · Cited by 125 · see citing works
Motivation: A Systematic Reinterpretation
Bindra, D. (1959) · Medical Entomology and Zoology · Cited by 124 · see citing works
Motivation: A Systematic Reinterpretation
Reider, N. (1960) · American Journal of Psychiatry · doi:10.1176/ajp.116.11.1051-b · Cited by 122 · see citing works
Attention-Like Processes in Drosophila Require Short-Term Memory Genes
van Swinderen, B. (2007) · Science · doi:10.1126/science.1137931 · Cited by 118 · see citing works
Appetite and Body Weight Regulation: Is It All in the Brain?
Kalra, S. P. (1997) · Neuron · doi:10.1016/s0896-6273(00)80934-4 · Cited by 114 · see citing works
Redrobe, J. P., Dumont, Y., Herzog, H., & Quirion, R. (2004) · Journal of Molecular Neuroscience · doi:10.1385/jmn:22:3:159 · Cited by 90 · see citing works
Peabody, N. C., Pohl, J. B., Diao, F., Vreede, A. P., Sandstrom, D. J., Wang, H., Zelensky, P. K., & White, B. H. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4241-08.2009 · Cited by 89 · see citing works
Self-citationStretch Receptors in the Foregut of the Blowfly
Gelperin, A. (1967) · Science · doi:10.1126/science.157.3785.208 · Cited by 87 · see citing works
Abdominal sensory neurons providing negative feedback to the feeding behavior of the blowfly
Gelperin, A. (1971) · Journal of Comparative Physiology A · doi:10.1007/bf00299201 · Cited by 79 · see citing works
Kohyama‐Koganeya, A., Kim, Y., Miura, M., & Hirabayashi, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807833105 · Cited by 65 · see citing works
Browning, K. N., & Travagli, R. A. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.042036 · Cited by 57 · see citing works
Role of Neuronal Glucosensing in the Regulation of Energy Homeostasis
Levin, B. E., Kang, L., Sanders, N. M., & Dunn-Meynell, A. A. (2006) · Diabetes · doi:10.2337/db06-s016 · Cited by 54 · see citing works
Sun, Q., Baraban, S. C., Prince, D. A., & Huguenard, J. R. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-29-09639.2003 · Cited by 53 · see citing works
Rhim, H., Kinney, G. A., Emmerson, P. J., & Miller, R. J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-09-02980.1997 · Cited by 49 · see citing works
Matheson, T. (2002) · Encyclopedia of Life Sciences · doi:10.1038/npg.els.0003637 · Cited by 29 · see citing works
Spontaneous Activity and Behavior
Roeder, K. D. (1955) · The Scientific monthly/Scientific monthly · Cited by 24 · see citing works
Suppression of excitatory cholinergic synaptic transmission by Drosophila dopamine D1‐like receptors
Yuan, N., & Lee, D. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05870.x · Cited by 24 · see citing works
Central control of movements and behavior of invertebrates
Huber, F. (1967) · MPG.PuRe (Max Planck Society) · Cited by 23 · see citing works
Animal Motivation: The Beginning of the End?
Kennedy, J. S. (1987) · Proceedings in life sciences · doi:10.1007/978-1-4612-4644-2_2 · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Dethier VG The Hungry Fly - a Physiological Study of the Behaviour 1976 Cambridge Harvard University Press
- Lorenz KZ The comparative method in studying innate behaviour patterns Physiological Mechanisms in Animal Behaviour 1950 Company of Biologists: Cambridge University Press
- Toates FM Motivational Systems 1986 Cambridge Cambridge University Press
Cited by
Sorted by citations
Reward and aversion in a heterogeneous midbrain dopamine system
Lammel, S., Lim, B. K., & Malenka, R. C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.019 · Cited by 804 · see citing works
Chiang, A.-S., Lin, C.-Y., Chuang, C.-C., Chang, H.-M., Hsieh, C.-H., Yeh, C.-W., Shih, C.-T., Wu, J.-J., Wang, G.-T., Chen, Y.-C., et al. (2011) · Current Biology · doi:10.1016/j.cub.2010.11.056 · Cited by 767 · see citing works
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 · see citing works
Self-citationPresynaptic facilitation by neuropeptide signaling mediates odor-driven food search
Root, C. M., Ko, K. I., Jafari, A., & Wang, J. W. (2011) · Cell · doi:10.1016/j.cell.2011.02.008 · Cited by 526 · see citing works
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila
Hige, T., Aso, Y., Modi, M. N., Rubin, G. M., & Turner, G. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.003 · Cited by 354 · see citing works
Inagaki, H. K., Ben-Tabou de-Leon, S., Wong, A. M., Jagadish, S., Ishimoto, H., Barnea, G., Kitamoto, T., Axel, R., & Anderson, D. J. (2012) · Cell · doi:10.1016/j.cell.2011.12.022 · Cited by 325 · see citing works
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 · see citing works
Cellular diversity in the Drosophila midbrain revealed by single-cell transcriptomics
Croset, V., Treiber, C. D., & Waddell, S. (2018) · eLife · doi:10.7554/elife.34550 · Cited by 299 · see citing works
Self-citationDopaminergic modulation of sucrose acceptance behavior in Drosophila
Marella, S., Mann, K., & Scott, K. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.032 · Cited by 240 · see citing works
Insects have the capacity for subjective experience
Klein, C., & Barron, A. B. (2016) · Animal Sentience · doi:10.51291/2377-7478.1113 · Cited by 243 · see citing works
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 233 · see citing works
“…Liu et al., 2009; Turner-Evans et al., 2020; Guo et al., 2016; Lu et al., 2022; Frenkel et al., 2017; Shafer et al., 2006; Senapati et al., 2019; Krashes et al., 2009; Busch et al., 2009; Liu et al., 2019; Dacks et al., 2006; Haynes et al., 2015; Hulse et al., 2021; Scheffer et al., 2020a) (see…”
Plasticity of local GABAergic interneurons drives olfactory habituation
Das, S., Sadanandappa, M. K., Dervan, A., Larkin, A., Lee, J. A., Sudhakaran, I. P., Priya, R., Heidari, R., Holohan, E. E., Pimentel, A., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106411108 · Cited by 219 · see citing works
Sexual Deprivation Increases Ethanol Intake in <i>Drosophila</i>
Shohat-Ophir, G., Kaun, K. R., Azanchi, R., Mohammed, H., & Heberlein, U. (2012) · Science · doi:10.1126/science.1215932 · Cited by 211 · see citing works
Tsao, C.-H., Chen, C.-C., Lin, C.-H., Yang, H.-Y., & Lin, S. (2018) · eLife · doi:10.7554/elife.35264 · Cited by 214 · see citing works
Memory-Relevant Mushroom Body Output Synapses Are Cholinergic
Barnstedt, O., Owald, D., Felsenberg, J., Brain, R., Moszynski, J.-P., Talbot, C. B., Perrat, P. N., & Waddell, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.015 · Cited by 197 · see citing works
Self-citationNeural Mechanisms of Reward in Insects
Perry, C. J., & Barron, A. B. (2013) · Annual Review of Entomology · doi:10.1146/annurev-ento-120811-153631 · Cited by 135 · see citing works
Aso, Y., Ray, R. P., Long, X., Bushey, D., Cichewicz, K., Ngo, T.-T., Sharp, B., Christoforou, C., Hu, A., Lemire, A. L., et al. (2019) · eLife · doi:10.7554/elife.49257 · Cited by 141 · see citing works
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 · see citing works
Fasting Launches CRTC to Facilitate Long-Term Memory Formation in <i>Drosophila</i>
Hirano, Y., Masuda, T., Naganos, S., Matsuno, M., Ueno, K., Miyashita, T., Horiuchi, J., & Saitoe, M. (2013) · Science · doi:10.1126/science.1227170 · Cited by 129 · see citing works
Scribble Scaffolds a Signalosome for Active Forgetting
Cervantes-Sandoval, I., Chakraborty, M., MacMullen, C., & Davis, R. L. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.010 · Cited by 100 · see citing works
Availability of food determines the need for sleep in memory consolidation
Chouhan, N. S., Griffith, L. C., Haynes, P., & Sehgal, A. (2021) · Nature · doi:10.1038/s41586-020-2997-y · Cited by 76 · see citing works
Gliotransmission of D-serine promotes thirst-directed behaviors in Drosophila
Park, A., Croset, V., Otto, N., Agarwal, D., Treiber, C. D., Meschi, E., Sims, D., & Waddell, S. (2022) · Current Biology · doi:10.1016/j.cub.2022.07.038 · Cited by 45 · see citing works
Self-citationPhenomenal interface theory: a model for basal consciousness
Klein, C., & Barron, A. B. (2025) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2024.0301 · Cited by 8 · see citing works
“In insects, small populations of aminergic cells signal aspects of the state of the insect and also provide reinforcement signals to the learning and memory centres of the mushroom bodies [69,70], so that the subjective meaning of objects in the environment to the organism can be learnt [70–72].”
- Authors
- Krashes, M. J., DasGupta, S., Vreede, A., White, B., Armstrong, J. D., & Waddell, S.
- Affiliations
- Harvard University (US)
- University of Massachusetts Chan Medical School (US)
- National Institutes of Health (US)
- University of Edinburgh (GB)
- Corresponding author
- Waddell, Scott
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2009-10
- Volume
- 139
- Issue
- 2
- Pages
- 416-427
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC2780032
- OpenAlex
- W2168414233
- Cited by
- 598
- References
- 96
- Citations by year
- 2026: 27 · 2025: 41 · 2024: 34 · 2023: 20 · 2022: 38 · 2021: 40 · 2020: 47 · 2019: 24 · 2018: 30 · 2017: 43 · 2016: 41 · 2015: 25 · 2014: 26 · 2013: 43 · 2012: 40
- FWCI
- 16.35
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1421 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- National Institutes of Health (1f31mh009883-01)
- National Institute of Mental Health (MH09883, R01MH069883, MH081982, R01MH081982)
- National Institute on Drug Abuse (DA024499, F31DA024499)
- 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
- appetitive memory, hunger, satiety, motivational states, neuropeptide F, dopamine, dopaminergic neurons, mushroom body, memory expression, food deprivation, Drosophila
- MeSH terms
- Animals, Appetitive Behavior, Behavior, Animal, Conditioning, Classical, Dopamine, Drosophila melanogaster, Memory, Motivation, Neuropeptides, Receptors, Neuropeptide, Mushroom Bodies, Drosophila Proteins
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
