Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior
Open accessAbstract
The fruit fly can evaluate its energy state and decide whether to pursue food-related cues. Here, we reveal that the mushroom body (MB) integrates hunger and satiety signals to control food-seeking behavior. We have discovered five pathways in the MB essential for hungry flies to locate and approach food. Blocking the MB-intrinsic Kenyon cells (KCs) and the MB output neurons (MBONs) in these pathways impairs food-seeking behavior. Starvation bi-directionally modulates MBON responses to a food odor, suggesting that hunger and satiety controls occur at the KC-to-MBON synapses. These controls are mediated by six types of dopaminergic neurons (DANs). By manipulating these DANs, we could inhibit food-seeking behavior in hungry flies or promote food seeking in fed flies. Finally, we show that the DANs potentially receive multiple inputs of hunger and satiety signals. This work demonstrates an information-rich central circuit in the fly brain that controls hunger-driven food-seeking behavior.
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?
Other aminergic systems associated with the mushroom bodies modify the neural output of the mushroom body such that food-associated stimuli are only attractive if an insect is food-deprived.
“For example, other aminergic systems associated with the mushroom bodies modify the neural output of the mushroom such that food-associated stimuli are only attractive if an insect is food-deprived [74].”
From Phenomenal interface theory: a model for basal consciousness (2025) · cites this paper as [74]
The Results sections on dopaminergic neurons and mushroom-body output neurons report that hunger-related dopamine signaling regulates flies’ food-seeking behavior and that starvation changes output-neuron responses to yeast odor. The paper also says hungry flies, rather than fed flies, approach yeast food. Its experiments concern fruit flies and yeast odor, so the claim’s broader wording about insects and food-associated stimuli is not established. (LLM, conf=0.84)
Experimental — accuracy not yet measured
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
Ultrasensitive fluorescent proteins for imaging neuronal activity
Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V., et al. (2013) · Nature · doi:10.1038/nature12354 · Cited by 6,474 · 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
Or83b Encodes a Broadly Expressed Odorant Receptor Essential for Drosophila Olfaction
Larsson, M. C., Domingos, A. I., Jones, W. D., Chiappe, M. E., Amrein, H., & Vosshall, L. B. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.019 · Cited by 1,411 · see citing works
Mushroom body memoir: from maps to models
Heisenberg, M. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1074 · Cited by 1,286 · 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
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
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 · see citing works
Kitamoto, T. (2001) · Journal of Neurobiology · doi:10.1002/neu.1018 · Cited by 868 · see citing works
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 · see citing works
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila
Aso, Y., Sitaraman, D., Ichinose, T., Kaun, K. R., Vogt, K., Belliart-Guérin, G., Plaçais, P.-Y., Robie, A. A., Yamagata, N., Schnaitmann, C., et al. (2014) · eLife · doi:10.7554/elife.04580 · Cited by 707 · see citing works
Jefferis, G. S. X. E., Potter, C. J., Chan, A. M., Marin, E. C., Torsten Rohlfing, B., Maurer, C. R., & Luo, L. (2007) · Cell · doi:10.1016/j.cell.2007.01.040 · Cited by 647 · see citing works
A subset of dopamine neurons signals reward for odour memory in Drosophila
Liu, C., Plaçais, P.-Y., Yamagata, N., Pfeiffer, B. D., Aso, Y., Friedrich, A. B., Siwanowicz, I., Rubin, G. M., Préat, T., & Tanimoto, H. (2012) · Nature · doi:10.1038/nature11304 · Cited by 623 · 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
A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila
Krashes, M. J., DasGupta, S., Vreede, A., White, B., Armstrong, J. D., & Waddell, S. (2009) · Cell · doi:10.1016/j.cell.2009.08.035 · Cited by 598 · see citing works
Functional Architecture of Olfactory Ionotropic Glutamate Receptors
Abuin, L., Bargeton, B., Ulbrich, M. H., Isacoff, E. Y., Kellenberger, S., & Benton, R. (2011) · Neuron · doi:10.1016/j.neuron.2010.11.042 · Cited by 580 · see citing works
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 · see citing works
Presynaptic 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
Rajan, A., & Perrimon, N. (2012) · Cell · doi:10.1016/j.cell.2012.08.019 · Cited by 499 · see citing works
Neuronal 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
Tripartite Mushroom Body Architecture Revealed by Antigenic MarkersPreprint
Crittenden, J. R., Skoulakis, E. M. C., Han, K., Kalderon, D., & Davis, R. L. (1998) · Learning & Memory · doi:10.1101/lm.5.1.38 · Cited by 446 · see citing works
Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila
Cohn, R., Morantte, I., & Ruta, V. (2015) · Cell · doi:10.1016/j.cell.2015.11.019 · Cited by 430 · see citing works
Regulation of Drosophila Life Span by Olfaction and Food-Derived Odors
Libert, S., Zwiener, J., Chu, X., VanVoorhies, W., Roman, G., & Pletcher, S. D. (2007) · Science · doi:10.1126/science.1136610 · Cited by 410 · see citing works
Random convergence of olfactory inputs in the Drosophila mushroom body
Caron, S. J. C., Ruta, V., Abbott, L. F., & Axel, R. (2013) · Nature · doi:10.1038/nature12063 · Cited by 409 · cited 3× · see citing works
“Each KC receives inputs from a random combination of antennal lobe projection neurons (Caron et al., 2013).”
BackgroundInfluentialDrosophila 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
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila
Owald, D., Felsenberg, J., Talbot, C. B., Das, G., Perisse, E., Huetteroth, W., & Waddell, S. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.025 · Cited by 367 · 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
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
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
Drosophila Short Neuropeptide F Regulates Food Intake and Body Size
Lee, K., You, K., Choo, J., Han, Y., & Yu, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407842200 · Cited by 348 · see citing works
Three Pillars for the Neural Control of Appetite
Sternson, S. M., & Eiselt, A.-K. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-104948 · Cited by 336 · 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
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
Specific Dopaminergic Neurons for the Formation of Labile Aversive Memory
Aso, Y., Siwanowicz, I., Bräcker, L. B., Ito, K., Kitamoto, T., & Tanimoto, H. (2010) · Current Biology · doi:10.1016/j.cub.2010.06.048 · Cited by 324 · see citing works
Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability
Aso, Y., Herb, A., Ogueta, M., Siwanowicz, I., Templier, T., Friedrich, A. B., Ito, K., Scholz, H., & Tanimoto, H. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002768 · Cited by 320 · see citing works
Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination
Lin, A. C., Bygrave, A. M., de Calignon, A., Lee, T., & Miesenböck, G. (2014) · Nature Neuroscience · doi:10.1038/nn.3660 · Cited by 317 · see citing works
A Drosophila Resource of Transgenic RNAi Lines for Neurogenetics
Ni, J., Liu, L., Binari, R. C., Hardy, R. W., Shim, H., Cavallaro, A., Booker, M. A., Pfeiffer, B. D., Markstein, M., Wang, H., et al. (2009) · Genetics · doi:10.1534/genetics.109.103630 · Cited by 311 · see citing works
Dopaminergic neurons write and update memories with cell-type-specific rules
Aso, Y., & Rubin, G. M. (2016) · eLife · doi:10.7554/elife.16135 · Cited by 306 · see citing works
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 296 · see citing works
DAMB, a Novel Dopamine Receptor Expressed Specifically in Drosophila Mushroom Bodies
Han, K., Millar, N. S., Grotewiel, M. S., & Davis, R. L. (1996) · Neuron · doi:10.1016/s0896-6273(00)80139-7 · Cited by 290 · see citing works
Distinct dopamine neurons mediate reward signals for short- and long-term memories
Yamagata, N., Ichinose, T., Aso, Y., Plaçais, P.-Y., Friedrich, A. B., Sima, R., Préat, T., Rubin, G. M., & Tanimoto, H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421930112 · Cited by 288 · 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
Cell-Type-Specific TEV Protease Cleavage Reveals Cohesin Functions in Drosophila Neurons
Pauli, A., Althoff, F., Oliveira, R. A., Heidmann, S. K., Schuldiner, O., Lehner, C. F., Dickson, B. J., & Nasmyth, K. (2008) · Developmental Cell · doi:10.1016/j.devcel.2007.12.009 · Cited by 276 · see citing works
Srivastava, D. P., Yu, E. J., Kennedy, K., Chatwin, H., Reale, V., Hamon, M., Smith, T., & Evans, P. D. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1005-05.2005 · Cited by 272 · see citing works
Nutrient Sensor in the Brain Directs the Action of the Brain-Gut Axis in Drosophila
Dus, M., Lai, J. S.-Y., Gunapala, K. M., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.032 · Cited by 267 · see citing works
Operation of a homeostatic sleep switch
Pimentel, D. O., Donlea, J. M., Talbot, C. B., Song, S. H., Thurston, A. J. F., & Miesenböck, G. (2016) · Nature · doi:10.1038/nature19055 · Cited by 267 · see citing works
Saudou, F., Boschert, U., Amlaiky, N., Plassat, J., & Hen, R. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05021.x · Cited by 266 · see citing works
Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila
Huetteroth, W., Perisse, E., Lin, S., Klappenbach, M., Burke, C., & Waddell, S. (2015) · Current Biology · doi:10.1016/j.cub.2015.01.036 · Cited by 265 · see citing works
Self-citationGenetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila
Nicolaï, L., Ramaekers, A., Raemaekers, T., Drozdzecki, A., Mauss, A. S., Yan, J., Landgraf, M., Annaert, W. G., & Hassan, B. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010198107 · Cited by 262 · see citing works
Gut hormones in the control of appetite
Murphy, K. G., & Bloom, S. R. (2004) · Experimental Physiology · doi:10.1113/expphysiol.2004.027789 · Cited by 251 · see citing works
Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila
Owald, D., & Waddell, S. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.10.002 · Cited by 251 · see citing works
The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning
Liu, X., & Davis, R. L. (2009) · Nature Neuroscience · doi:10.1038/nn.2235 · Cited by 250 · see citing works
Dopaminergic 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
Hoopfer, E. D., Jung, Y., Inagaki, H., Rubin, G. M., & Anderson, D. J. (2015) · eLife · doi:10.7554/elife.11346 · Cited by 235 · see citing works
Ko, K. I., Root, C. M., Lindsay, S. A., Zaninovich, O. A., Shepherd, A. K., Wasserman, S. A., Kim, S. M., & Wang, J. W. (2015) · eLife · doi:10.7554/elife.08298 · Cited by 231 · see citing works
Hearn, M. G., Ren, Y., McBride, E. W., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202498299 · Cited by 230 · see citing works
Leptin and Insulin Action in the Central Nervous System
Porte, D., Baskin, D. G., & Schwartz, M. W. (2002) · Nutrition Reviews · doi:10.1301/002966402320634797 · Cited by 229 · see citing works
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 · see citing works
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 · see citing works
Perisse, E., Owald, D., Barnstedt, O., Talbot, C. B., Huetteroth, W., & Waddell, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.04.034 · Cited by 216 · see citing works
Inagaki, H. K., Panse, K. M., & Anderson, D. J. (2014) · Neuron · doi:10.1016/j.neuron.2014.09.032 · Cited by 214 · see citing works
Allatostatin-A neurons inhibit feeding behavior in adult Drosophila
Hergarden, A. C., Tayler, T. D., & Anderson, D. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200778109 · Cited by 214 · see citing works
Neural correlates of water reward in thirsty Drosophila
Lin, S., Owald, D., Chandra, V., Talbot, C. B., Huetteroth, W., & Waddell, S. (2014) · Nature Neuroscience · doi:10.1038/nn.3827 · Cited by 213 · see citing works
Self-citationUpregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory
Plaçais, P.-Y., de Tredern, É., Scheunemann, L., Trannoy, S., Goguel, V., Han, K.-A., Isabel, G., & Préat, T. (2017) · Nature Communications · doi:10.1038/ncomms15510 · Cited by 211 · see citing works
Gamma Neurons Mediate Dopaminergic Input during Aversive Olfactory Memory Formation in Drosophila
Qin, H., Cressy, M., Li, W., Coravos, J. S., Izzi, S. A., & Dubnau, J. (2012) · Current Biology · doi:10.1016/j.cub.2012.02.014 · Cited by 205 · see citing works
The Role of Dopamine in Drosophila Larval Classical Olfactory Conditioning
Selcho, M., Pauls, D., Han, K.-A., Stocker, R. F., & Thum, A. S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005897 · Cited by 202 · 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
A Syd-1 homologue regulates pre- and postsynaptic maturation in <i>Drosophila</i>
Owald, D., Fouquet, W., Schmidt, M., Wichmann, C., Mertel, S., Depner, H., Christiansen, F., Zube, C., Quentin, C., Körner, J., et al. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200908055 · Cited by 191 · see citing works
A Deceptive Pollination System Targeting Drosophilids through Olfactory Mimicry of Yeast
Stökl, J., Strutz, A., Dafni, A., Svatoš, A., Doubský, J., Knaden, M., Sachse, S., Hansson, B. S., & Stensmyr, M. C. (2010) · Current Biology · doi:10.1016/j.cub.2010.09.033 · Cited by 191 · see citing works
Heimbeck, G., Bugnon, V., Gendre, N., Keller, A., & Stocker, R. F. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.011314898 · Cited by 187 · see citing works
Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila
Plaçais, P.-Y., Trannoy, S., Isabel, G., Aso, Y., Siwanowicz, I., Belliart-Guérin, G., Vernier, P., Birman, S., Tanimoto, H., & Préat, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3055 · Cited by 178 · see citing works
Insulin controls food intake and energy balance via NPY neurons
Loh, K., Zhang, L., Brandon, A. E., Wang, Q., Begg, D. P., Qi, Y., Fu, M., Kulkarni, R. N., Teo, J. D., Baldock, P. A. J., et al. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.03.013 · Cited by 173 · see citing works
Feeding regulation in Drosophila
Pool, A., & Scott, K. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.05.008 · Cited by 167 · see citing works
Regulation of starvation-induced hyperactivity by insulin and glucagon signaling in adult Drosophila
Yu, Y., Huang, R., Ye, J., Zhang, V., Wu, C., Cheng, G., Jia, J., & Wang, L. (2016) · eLife · doi:10.7554/elife.15693 · Cited by 167 · see citing works
Reward signal in a recurrent circuit drives appetitive long-term memory formation
Ichinose, T., Aso, Y., Yamagata, N., Abe, A., Rubin, G. M., & Tanimoto, H. (2015) · eLife · doi:10.7554/elife.10719 · Cited by 162 · see citing works
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila
Lewis, L., Siju, K. P., Aso, Y., Friedrich, A. B., Bulteel, A. J. B., Rubin, G. M., & Kadow, I. C. G. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.015 · Cited by 161 · see citing works
Decoding odor quality and intensity in the Drosophila brain
Strutz, A., Sölter, J., Baschwitz, A., Farhan, A., Grabe, V., Rybak, J., Knaden, M., Schmuker, M., Hansson, B. S., & Sachse, S. (2014) · eLife · doi:10.7554/elife.04147 · Cited by 157 · see citing works
Plasticity-driven individualization of olfactory coding in mushroom body output neurons
Hige, T., Aso, Y., Rubin, G. M., & Turner, G. C. (2015) · Nature · doi:10.1038/nature15396 · Cited by 157 · see citing works
Strausfeld, N. J., Sinakevitch, I. G., & Vilinsky, I. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10368 · Cited by 155 · see citing works
Re-evaluation of learned information in Drosophila
Felsenberg, J., Barnstedt, O., Cognigni, P., Lin, S., & Waddell, S. (2017) · Nature · doi:10.1038/nature21716 · Cited by 155 · see citing works
Self-citationCoupled sensing of hunger and thirst signals balances sugar and water consumption
Jourjine, N., Mullaney, B. C., Mann, K., & Scott, K. (2016) · Cell · doi:10.1016/j.cell.2016.06.046 · Cited by 154 · see citing works
Scheidler, N. H., Liu, C., Hamby, K. A., Zalom, F. G., & Syed, Z. (2015) · Scientific Reports · doi:10.1038/srep14059 · Cited by 152 · see citing works
Synaptic transmission parallels neuromodulation in a central food-intake circuit
Schlegel, P., Texada, M. J., Miroschnikow, A., Schoofs, A., Hückesfeld, S., Peters, M., Schneider-Mizell, C. M., Lacin, H., Li, F., Fetter, R. D., et al. (2016) · eLife · doi:10.7554/elife.16799 · Cited by 151 · see citing works
Gotzes, F., Balfanz, S., & Baumann, A. (1994) · PubMed · Cited by 150 · see citing works
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 · see citing works
The Neural Circuitry that Functions as a Switch for Courtship versus Aggression in Drosophila Males
Koganezawa, M., Kimura, K.-I., & Yamamoto, D. (2016) · Current Biology · doi:10.1016/j.cub.2016.04.017 · Cited by 147 · see citing works
Sensory integration and neuromodulatory feedback facilitate Drosophila mechanonociceptive behavior
Hu, C., Petersen, M., Hoyer, N., Spitzweck, B., Tenedini, F. M., Wang, D., Gruschka, A., Burchardt, L. S., Szpotowicz, E., Schweizer, M., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4580 · Cited by 133 · see citing works
Ancient anxiety pathways influence drosophila defense behaviors
Mohammad, F., Aryal, S., Ho, J., Stewart, J. C., Norman, N. A., Tan, T. L., Eisaka, A., & Claridge-Chang, A. (2016) · Current Biology · doi:10.1016/j.cub.2016.02.031 · Cited by 130 · see citing works
Representations of Novelty and Familiarity in a Mushroom Body Compartment
Hattori, D., Aso, Y., Swartz, K. J., Rubin, G. M., Abbott, L. F., & Axel, R. (2017) · Cell · doi:10.1016/j.cell.2017.04.028 · Cited by 130 · 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
Branch-specific plasticity of a bifunctional dopamine circuit encodes protein hunger
Liu, Q., Tabuchi, M., Liu, S., Kodama, L., Horiuchi, W., Daniels, J., Chiu, L. T., Baldoni, D., & Wu, M. N. (2017) · Science · doi:10.1126/science.aal3245 · Cited by 128 · see citing works
Odor Discrimination in Drosophila: From Neural Population Codes to Behavior
Parnas, M., Lin, A. C., Huetteroth, W., & Miesenböck, G. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.006 · Cited by 126 · 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
Hong, S.-H., Lee, K., Kwak, S., Kim, A., Bai, H., Jung, M., Kwon, O., Song, W., Tatar, M., & Yu, K. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002857 · Cited by 123 · see citing works
Plaçais, P.-Y., Trannoy, S., Friedrich, A. B., Tanimoto, H., & Préat, T. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.09.032 · Cited by 123 · see citing works
Pai, T.-P., Chen, C.-C., Lin, H., Chin, A., Lai, J. S.-Y., Lee, P.-T., Tully, T., & Chiang, A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216336110 · Cited by 118 · see citing works
Self-citationGut hormones and the control of appetite
SMALL, C., & Bloom, S. (2004) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2004.06.002 · Cited by 118 · see citing works
Starvation-Induced Depotentiation of Bitter Taste in Drosophila
LeDue, E. E., Mann, K. J., Koch, E. T., Chu, B., Dakin, R., & Gordon, M. D. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.028 · Cited by 116 · see citing works
Suppression of Dopamine Neurons Mediates Reward
Yamagata, N., Hiroi, M., Kondo, S., Abe, A., & Tanimoto, H. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002586 · Cited by 113 · see citing works
Neural circuits and motivational processes for hunger
Sternson, S. M., Nicholas Betley, J., & Cao, Z. F. H. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.04.006 · Cited by 108 · see citing works
Drosophila FIT is a protein-specific satiety hormone essential for feeding control
Sun, J., Liu, C. X., Bai, X., Li, X., Li, J., Zhang, Z., Zhang, Y., Guo, J., & Li, Y. (2017) · Nature Communications · doi:10.1038/ncomms14161 · Cited by 108 · see citing works
Essential Role of the Mushroom Body in Context-Dependent CO2 Avoidance in Drosophila
Bräcker, L. B., Siju, K. P., Varela, N., Aso, Y., Zhang, M., Hein, I., Vasconcelos, M. L., & Kadow, I. C. G. (2013) · Current Biology · doi:10.1016/j.cub.2013.05.029 · Cited by 107 · see citing works
FoxP influences the speed and accuracy of a perceptual decision in Drosophila
Dasgupta, S., Ferreira, C. H., & Miesenböck, G. (2014) · Science · doi:10.1126/science.1252114 · Cited by 102 · see citing works
Drosophila Learn Opposing Components of a Compound Food Stimulus
Das, G., Klappenbach, M., Vrontou, E., Perisse, E., Clark, C. M., Burke, C. J., & Waddell, S. (2014) · Current Biology · doi:10.1016/j.cub.2014.05.078 · Cited by 102 · see citing works
Gorter, J. A., Jagadeesh, S., Gahr, C. L., et al. (2016) · Scientific Reports · doi:10.1038/srep19441 · Cited by 97 · see citing works
Cervantes-Sandoval, I., Phan, A., Chakraborty, M., & Davis, R. L. (2017) · eLife · doi:10.7554/elife.23789 · Cited by 96 · see citing works
A Subset of Serotonergic Neurons Evokes Hunger in Adult Drosophila
Albin, S. D., Kaun, K. R., Knapp, J.-M., Chung, P., Heberlein, U., & Simpson, J. H. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.005 · Cited by 95 · see citing works
Converging Circuits Mediate Temperature and Shock Aversive Olfactory Conditioning in Drosophila
Galili, D. S., Dylla, K. V., Lüdke, A., Friedrich, A. B., Yamagata, N., Wong, J. Y. H., Ho, C. H., Szyszka, P., & Tanimoto, H. (2014) · Current Biology · doi:10.1016/j.cub.2014.06.062 · Cited by 95 · see citing works
The CCHamide 1 receptor modulates sensory perception and olfactory behavior in starved Drosophila
Farhan, A., Gulati, J., Große‐Wilde, E., Vogel, H., Hansson, B. S., & Knaden, M. (2013) · Scientific Reports · doi:10.1038/srep02765 · Cited by 92 · see citing works
Delayed Dopamine Signaling of Energy Level Builds Appetitive Long-Term Memory in Drosophila
Musso, P., Tchénio, P., & Préat, T. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.036 · Cited by 92 · see citing works
Neuropeptide-Gated Perception of Appetitive Olfactory Inputs in Drosophila Larvae
Wang, Y., Pu, Y., & Shen, P. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.02.003 · Cited by 87 · see citing works
Wang, Y., Chiang, A., Xia, S., Kitamoto, T., Tully, T., & Zhong, Y. (2003) · Current Biology · doi:10.1016/j.cub.2003.10.003 · Cited by 82 · see citing works
cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila
Hong, S.-T., Bang, S., Hyun, S., Kang, J., Jeong, K., Paik, D., Chung, J., & Kim, J. (2008) · Nature · doi:10.1038/nature07090 · Cited by 79 · see citing works
Graded Encoding of Food Odor Value in theDrosophilaBrain
Beshel, J., & Zhong, Y. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2605-13.2013 · Cited by 77 · see citing works
Beshel, J., Dubnau, J., & Zhong, Y. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2016.12.013 · Cited by 73 · see citing works
Dopamine Signalling in Mushroom Bodies Regulates Temperature-Preference Behaviour in Drosophila
Bang, S., Hyun, S., Hong, S.-T., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001346 · Cited by 72 · see citing works
Kaneko, T., Macara, A. M., Li, R., Hu, Y., Iwasaki, K., Dunnings, Z., Firestone, E., Horvatic, S., Guntur, A. R., Shafer, O. T., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.034 · Cited by 63 · see citing works
Neural circuits for long-term water-reward memory processing in thirsty Drosophila
Shyu, W.-H., Chiu, T.-H., Chiang, M.-H., Cheng, Y.-C., Tsai, Y.-L., Fu, T., Wu, T., & Wu, C. (2017) · Nature Communications · doi:10.1038/ncomms15230 · Cited by 60 · see citing works
Lenz, C., Søndergaard, L., & Grimmelikhuijzen, C. J. P. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.2251 · Cited by 57 · see citing works
Li, H. L., Roch, J., Sundsmo, M. P., Otero, D. A. C., Sisodia, S. S., Thomas, R. G., & Saitoh, T. (1997) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199705)32:5 · Cited by 56 · see citing works
Behavioral Modulation by Spontaneous Activity of Dopamine Neurons
Ichinose, T., Tanimoto, H., & Yamagata, N. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00088 · Cited by 36 · see citing works
Ueoka, Y., Hiroi, M., Abe, T., & Tabata, T. (2017) · FEBS Open Bio · doi:10.1002/2211-5463.12203 · Cited by 35 · see citing works
Role of gastrointestinal hormones in feeding behavior and obesity treatment
Kairupan, T. S., Amitani, H., Cheng, K., Runtuwene, J., Asakawa, A., & Inui, A. (2015) · Journal of Gastroenterology · doi:10.1007/s00535-015-1118-4 · Cited by 29 · see citing works
Parallel circuits control temperature preference in Drosophila during ageing
Shih, H.-W., Wu, C., Chang, S.-W., Liu, T.-H., Lai, J. S.-Y., Fu, T., Fu, C., & Chiang, A. (2015) · Nature Communications · doi:10.1038/ncomms8775 · Cited by 27 · see citing works
GABAA receptor-expressing neurons promote consumption in Drosophila melanogaster
Cheung, S. K., & Scott, K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175177 · Cited by 27 · see citing works
A fat-derived metabolite regulates a peptidergic feeding circuit in Drosophila
Kim, D., Shin, M., Jung, S., Kim, Y., & Jones, W. D. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2000532 · Cited by 26 · see citing works
Wang, C.-H., Huang, Y., Chen, P., Cheng, Y.-J., Kao, H.-H., Pi, H., & Chien, C. (2017) · eLife · doi:10.7554/elife.26886 · Cited by 21 · see citing works
Active Forgetting of Olfactory Memories in Drosophila
Berry, J. A., & Davis, R. L. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63350-7.00002-4 · Cited by 20 · see citing works
Yoshihara, M. (2012) · Journal of Visualized Experiments · doi:10.3791/3625 · Cited by 18 · see citing works
Neural mechanisms of context-dependent processing of CO 2 avoidance behavior in fruit flies
Siju, K. P., Bräcker, L. B., & Kadow, I. C. G. (2014) · Fly · doi:10.4161/fly.28000 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Tastekin, I., Khandelwal, A., Tadres, D., Fessner, N. D., Truman, J. W., Zlatic, M., Cardona, A., & Louis, M. (2018) · eLife · doi:10.7554/elife.38740 · Cited by 78 · see citing works
Behavioral dissection of hunger states in Drosophila
Weaver, K. J., Raju, S., Rucker, R. A., Chakraborty, T., Holt, R. A., & Pletcher, S. D. (2023) · eLife · doi:10.7554/elife.84537.3 · Cited by 13 · see citing works
Phenomenal 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
“For example, other aminergic systems associated with the mushroom bodies modify the neural output of the mushroom such that food-associated stimuli are only attractive if an insect is food-deprived [74].”
- Authors
- Tsao, C.-H., Chen, C.-C., Lin, C.-H., Yang, H.-Y., & Lin, S.
- Affiliations
- Institute of Molecular Biology, Academia Sinica (TW)
- Corresponding author
- Lin, Suewei
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2018-03-16
- Volume
- 7
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5910021
- OpenAlex
- W2790008006
- Cited by
- 214
- References
- 131
- Citations by year
- 2026: 26 · 2025: 28 · 2024: 36 · 2023: 33 · 2022: 22 · 2021: 26 · 2020: 20 · 2019: 16 · 2018: 7
- FWCI
- 7.85
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Ministry of Science and Technology, Taiwan (105-2628-B-001-005-MY3)
- Academia Sinica
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- mushroom body, hunger, satiety, food-seeking behavior, Kenyon cells, mushroom body output neurons, dopaminergic neurons, starvation, food odor, energy state, Drosophila, neural circuits
- MeSH terms
- Animals, Appetitive Behavior, Brain, Drosophila melanogaster, Feeding Behavior, Food, Hunger, Instinct, Satiety Response, Starvation, Gene Expression, Mushroom Bodies, Drosophila Proteins, Dopaminergic Neurons
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