Persistent activity in a recurrent circuit underlies courtship memory in Drosophila
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Recurrent connections are thought to be a common feature of the neural circuits that encode memories, but how memories are laid down in such circuits is not fully understood. Here we present evidence that courtship memory in Drosophila relies on the recurrent circuit between mushroom body gamma (MBγ), M6 output, and aSP13 dopaminergic neurons. We demonstrate persistent neuronal activity of aSP13 neurons and show that it transiently potentiates synaptic transmission from MBγ>M6 neurons. M6 neurons in turn provide input to aSP13 neurons, prolonging potentiation of MBγ>M6 synapses over time periods that match short-term memory. These data support a model in which persistent aSP13 activity within a recurrent circuit lays the foundation for a short-term memory.
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Central excitatory glutamatergic transmission has also been reported.
“However, central excitatory glutamatergic transmission has also been reported.93,95,116,117”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [95]
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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
The molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917 · see citing works
Neocortical excitation/inhibition balance in information processing and social dysfunction
Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O’Shea, D. J., Sohal, V. S., Goshen, I., Finkelstein, J., Paz, J. T., et al. (2011) · Nature · doi:10.1038/nature10360 · Cited by 2,454 · see citing works
Independent optical excitation of distinct neural populations
Klapoetke, N. C., Murata, Y., Kim, S. S., Pulver, S. R., Birdsey-Benson, A., Cho, Y. K., Morimoto, T. K., Chuong, A. S., Carpenter, E. J., Tian, Z., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2836 · Cited by 2,344 · see citing works
Synaptic reverberation underlying mnemonic persistent activity
Wang, X.-J. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01868-3 · Cited by 1,059 · 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
Tools for neuroanatomy and neurogenetics in Drosophila
Pfeiffer, B. D., Jenett, A., Hammonds, A. S., Ngo, T.-T. B., Misra, S., Murphy, C., Scully, A. L., Carlson, J. W., Wan, K. H., Laverty, T., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803697105 · Cited by 974 · 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
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 · see citing works
Cascade Models of Synaptically Stored Memories
Fusi, S., Drew, P. J., & Abbott, L. F. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.001 · Cited by 569 · see citing works
Mao, Z. (2009) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.005.2009 · Cited by 532 · see citing works
The complete connectome of a learning and memory centre in an insect brain
Eichler, K., Li, F., Litwin-Kumar, A., Park, Y., Andrade, I. V., Schneider-Mizell, C. M., Saumweber, T., Huser, A., Eschbach, C., Gerber, B., et al. (2017) · Nature · doi:10.1038/nature23455 · Cited by 494 · see citing works
Conditioned responses in courtship behavior of normal and mutant Drosophila
Siegel, R. W., & Hall, J. C. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.7.3430 · Cited by 488 · see citing works
Ultra light-sensitive and fast neuronal activation with the Ca2+-permeable channelrhodopsin CatCh
Kleinlogel, S., Feldbauer, K., Dempski, R. E., Fotis, H., Wood, P. G., Bamann, C., & Bamberg, E. (2011) · Nature Neuroscience · doi:10.1038/nn.2776 · Cited by 477 · see citing works
The control of sexual receptivity in female Drosophila
Manning, A. (1967) · Animal Behaviour · doi:10.1016/0003-3472(67)90006-1 · Cited by 476 · see citing works
Electrical Silencing of Drosophila Pacemaker Neurons Stops the Free-Running Circadian Clock
Nitabach, M. N., Blau, J., & Holmes, T. C. (2002) · Cell · doi:10.1016/s0092-8674(02)00737-7 · Cited by 452 · 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
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 1× · see citing works
“But MBg neurons likely do not specifically respond to cVA (Caron et al., 2013; Gruntman and Turner, 2013), so this change alone cannot account for the enhanced sensitivity of trained flies to cVA.”
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
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
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
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
The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxisPreprint
Rosenzweig, M. R., Brennan, K. M., Tayler, T. D., Phelps, P. O., Patapoutian, A., & Garrity, P. (2005) · Genes & Development · doi:10.1101/gad.1278205 · Cited by 323 · 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
Davis, R. L. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.012 · Cited by 290 · see citing works
Function of the Drosophila CPEB protein Orb2 in long-term courtship memory
Keleman, K., Krüttner, S., Alenius, M., & Dickson, B. J. (2007) · Nature Neuroscience · doi:10.1038/nn1996 · Cited by 266 · see citing works
Self-citationMushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila
Séjourné, J., Plaçais, P.-Y., Aso, Y., Siwanowicz, I., Trannoy, S., Thoma, V., Tedjakumala, S. R., Rubin, G. M., Tchénio, P., Ito, K., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2846 · Cited by 265 · see citing works
McBride, S. M. J., Giuliani, G., Choi, C. H., Krause, P., Correale, D., Watson, K. K., Baker, G., & Siwicki, K. K. (1999) · Neuron · doi:10.1016/s0896-6273(00)81043-0 · Cited by 261 · see citing works
Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs
Sun, W., Tan, Z., Mensh, B. D., & Ji, N. (2015) · Nature Neuroscience · doi:10.1038/nn.4196 · Cited by 231 · 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
Dopamine neurons modulate pheromone responses in Drosophila courtship learning
Keleman, K., Vrontou, E., Krüttner, S., Yu, J. Y., Kurtović-Kozarić, A., & Dickson, B. J. (2012) · Nature · doi:10.1038/nature11345 · Cited by 216 · see citing works
Self-citationPerisse, 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
Conditional modulation of spike-timing-dependent plasticity for olfactory learning
Cassenaer, S., & Laurent, G. (2012) · Nature · doi:10.1038/nature10776 · Cited by 215 · 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
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
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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 190 · see citing works
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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
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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
Integration of the olfactory code across dendritic claws of single mushroom body neurons
Gruntman, E., & Turner, G. C. (2013) · Nature Neuroscience · doi:10.1038/nn.3547 · Cited by 151 · see citing works
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Tompkins, L. (1984) · Behavior Genetics · doi:10.1007/bf01065443 · Cited by 147 · see citing works
Cholinergic Synaptic Transmission in AdultDrosophilaKenyon CellsIn Situ
Gu, H., & O’Dowd, D. K. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4109-05.2006 · Cited by 144 · 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
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
Drosophila Conditioned Courtship: Two Ways of Testing MemoryPreprint
Камышев, Н. Г., Iliadi, K. G., & Bragina, J. V. (1999) · Learning & Memory · doi:10.1101/lm.6.1.1 · Cited by 118 · see citing works
Synaptic Orb2A Bridges Memory Acquisition and Late Memory Consolidation in Drosophila
Krüttner, S., Traunmüller, L., Dag, U., Jandrasits, K., Stepien, B. K., Iyer, N., Fradkin, L. G., Noordermeer, J. N., Mensh, B. D., & Keleman, K. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.05.037 · Cited by 83 · see citing works
Self-citationAssociative learning and memory in Drosophila: beyond olfactory conditioning
Siwicki, K. K., & Ladewski, L. (2003) · Behavioural Processes · doi:10.1016/s0376-6357(03)00137-2 · Cited by 69 · see citing works
Kitamoto, T. (2002) · Journal of Neurogenetics · doi:10.1080/01677060216295 · Cited by 66 · see citing works
Martin, J., Keller, A., & Sweeney, S. T. (2002) · Advances in genetics · doi:10.1016/s0065-2660(02)47001-0 · Cited by 56 · see citing works
Montague, S. A., & Baker, B. S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164516 · Cited by 43 · see citing works
Sex Determination: Sex on the Brain?
Wolfner, M. F. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00038-1 · Cited by 13 · see citing works
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de Queiroz, B. R., Laghrissi, H., Rajeev, S., Blot, L., Graeve, F. D., Dehecq, M., Hallegger, M., Dag, U., de Segonzac, M. D., Ramialison, M., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57651-7 · Cited by 12 · see citing works
Self-citationMultilevel feedback architecture for adaptive regulation of learning in the insect brainPreprint
Eschbach, C., Fushiki, A., Winding, M., Schneider-Mizell, C. M., Shao, M., Arruda, R., Eichler, K., Valdés-Alemán, J., Ohyama, T., Thum, A. S., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/649731 · Cited by 11 · see citing works
Sleep benefits different stages of memory in Drosophila
Marquand, K., Roselli, C., Cervantes-Sandoval, I., & Boto, T. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1087025 · Cited by 9 · see citing works
A neural circuit arbitrates between perseverance and withdrawal in hungry DrosophilaPreprint
Sayın, S., Backer, J. D., Wosniack, M. E., Lewis, L., Siju, K. P., Frisch, L. M., Schlegel, P., Edmondson-Stait, A. J., Sharifi, N., Fisher, C. B., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/259119 · Cited by 9 · see citing works
Adel, M., Chen, N., Zhang, Y., Reed, M. L., Quasney, C., & Griffith, L. C. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0144-22.2022 · Cited by 8 · see citing works
Raun, N., Jones, S. G., Kerr, O., Keung, C., Butler, E. F., Alka, K., Krupski, J. D., Reid-Taylor, R. A., Ibrahim, V., Williams, M., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003004 · Cited by 6 · see citing works
A memory transcriptome time course reveals essential long-term memory transcription factors
Jones, S. G., Gil-Martí, B., Sacristán-Horcajada, E., Edison, A., Butler, E. F., Miandashti, N., Roselli, C., Turiégano, E., Boto, T., Kramer, J. M., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-64379-x · Cited by 5 · see citing works
Zhuravlev, A. V., Ivanova, P. N., Makaveeva, K. A., Zakharov, G. A., Nikitina, E. A., & Savvateeva-Popova, E. V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012356 · Cited by 5 · see citing works
Effect of impaired kynurenine synthesis on memory in Drosophila
Nikitina, E. A., Zhuravlev, A. V., & Savvateeva-Popova, E. V. (2021) · Integrative Physiology · doi:10.33910/2687-1270-2021-2-1-49-60 · Cited by 5 · see citing works
Learning with reward prediction errors in a model of the Drosophila mushroom bodyPreprint
Bennett, J., Philippides, A. O., & Nowotny, T. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/776401 · Cited by 5 · see citing works
Arginine kinase interacts with 2MIT and is involved in Drosophila melanogaster short-term memory
Bozzato, A., Romoli, O., Polo, D., Baggio, F., Mazzotta, G. M., Triolo, G., Myers, M. P., & Sandrelli, F. (2020) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2020.104118 · Cited by 4 · see citing works
Courtship suppression in Drosophila melanogaster: The role of mating failure
Goncharova, A. A., Besedina, N. G., Bragina, J. V., Danilenkova, L. V., Аркадьевна, К. Е., & Fedotov, S. A. (2023) · PLoS ONE · doi:10.1371/journal.pone.0290048 · Cited by 4 · see citing works
New genetic tools for mushroom body output neurons in Drosophila
Rubin, G. M., & Aso, Y. (2024) · eLife · doi:10.7554/elife.90523.3 · Cited by 4 · see citing works
Dopamine neurons promotes wakefulness via the DopR receptor in the Drosophila mushroom bodyPreprint
Driscoll, M., Buchert, S. N., Coleman, V., McLaughlin, M., Nguyen, A., & Sitaraman, D. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.29.069229 · Cited by 4 · see citing works
New genetic tools for mushroom body output neurons in DrosophilaPreprint
Rubin, G. M., & Aso, Y. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.23.546330 · Cited by 4 · see citing works
Roles of feedback and feed-forward networks of dopamine subsystems: insights fromDrosophilastudiesPreprint
Davidson, A. M., & Hige, T. (2024) · Learning & Memory · doi:10.1101/lm.053807.123 · Cited by 4 · see citing works
Brovero, S. G., Fortier, J. C., Hu, H., Lovejoy, P. C., Newell, N. R., Palmateer, C. M., Tzeng, R.-Y., Lee, P.-T., Zinn, K., & Arbeitman, M. N. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.02.323477 · Cited by 3 · see citing works
Pribbenow, C., Chen, Y., Heim, M. ‐., Laber, D., Reubold, S., Reynolds, E., Balles, I. S., Suárez-Grimalt, R., Rauch, C., Rösner, J., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.01.450776 · Cited by 3 · see citing works
The role of dopaminergic neuronal clusters in governing division of labor in ants
Zhong, W., Xie, N., Ding, G., Zhao, J., Zhang, P., Li, Q., Ran, H., Zhang, G., & Liu, W. (2025) · Insect Science · doi:10.1111/1744-7917.70087 · Cited by 4 · see citing works
Zhuravlev, A. V., Vetrovoy, O. V., Zalomaeva, E. S., Egozova, E. S., Nikitina, E. A., & Savvateeva-Popova, E. V. (2024) · Biochemistry (Moscow) · doi:10.1134/s0006297924030015 · Cited by 2 · see citing works
A positive feedback loop promotes the active internal state of the C. elegans egg-laying circuit
Prashad, S., Davison, C. A., Hammarlund, M., & Koelle, M. R. (2025) · Current Biology · doi:10.1016/j.cub.2025.10.005 · Cited by 1 · see citing works
Zhuravlev, A. V., Zalomaeva, E. S., Egozova, E. S., Emelin, A. D., Sokurova, V. V., Nikitina, E. A., & Savvateeva-Popova, E. V. (2023) · Vavilov Journal of Genetics and Breeding · doi:10.18699/vjgb-23-31 · Cited by 1 · see citing works
Neuroscience: Tantalized Flies Are Primed for Satiety
Ahmed, O. M., & Murthy, M. (2019) · Current Biology · doi:10.1016/j.cub.2019.09.029 · Cited by 1 · see citing works
Fedotov, S. A., Besedina, N. G., Bragina, J. V., Danilenkova, L. V., Аркадьевна, К. Е., & Камышев, Н. Г. (2020) · Integrative Physiology · doi:10.33910/2687-1270-2020-1-4-365-378 · Cited by 1 · see citing works
New genetic tools for mushroom body output neurons in DrosophilaPreprint
Rubin, G. M., & Aso, Y. (2023) · eLife · doi:10.7554/elife.90523.1 · Cited by 1 · see citing works
Schwartz, S., Wilson, S. J., Hale, T. K., & Fitzsimons, H. L. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.18.452850
Mohammad, F., Mai, Y., Ho, J., Zhang, X., Ott, S., Stewart, J. C., & Claridge‐Chang, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.23.517775
New genetic tools for mushroom body output neurons in DrosophilaPreprint
Rubin, G. M., & Aso, Y. (2024) · eLife · doi:10.7554/elife.90523.2
Homosensory and heterosensory dishabituation engage distinct circuits in DrosophilaPreprint
Charonitakis, A., Pasadaki, S., Georganta, E., Foka, K., Σεμελίδου, Ο., & Skoulakis, E. M. C. (2025) · eLife · doi:10.7554/elife.106322.1
Homosensory and heterosensory dishabituation engage distinct circuits in DrosophilaPreprint
Charonitakis, A., Pasadaki, S., Georganta, E., Foka, K., Σεμελίδου, Ο., & Skoulakis, E. M. C. (2025) · eLife · doi:10.7554/elife.106322
Striking parallels between the dopaminergic systems of flies and mammals
Jovanoski, K. D., & Waddell, S. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-29867-7.00025-6
Ventimiglia, D., Chamiec-Case, E., Lee, C. S., Ruff, B., & Asahina, K. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.20.706896
Divergent spatiotemporal integration of whole-field visual motion in medaka and zebrafish larvaePreprint
Isoe, Y., Mabene, Y. F., Bind, M.-A., & Engert, F. (2026) · eLife · doi:10.7554/elife.111462
Divergent spatiotemporal integration of whole-field visual motion in medaka and zebrafish larvaePreprint
Isoe, Y., Mabene, Y. F., Bind, M.-A., & Engert, F. (2026) · eLife · doi:10.7554/elife.111462.1
- Authors
- Zhao, X., Lenek, D., Dag, U., Dickson, B. J., & Keleman, K.
- Affiliations
- Howard Hughes Medical Institute (US)
- Research Institute of Molecular Pathology (AT)
- Corresponding author
- Keleman, Krystyna
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2018-01-11
- Volume
- 7
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5800849
- OpenAlex
- W2783309950
- Cited by
- 74
- References
- 53
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 7 · 2023: 10 · 2022: 8 · 2021: 8 · 2020: 14 · 2019: 10 · 2018: 6
- FWCI
- 4.33
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Howard Hughes Medical Institute
- Boehringer Ingelheim
- Austrian Science Fund (FWF P24499)
- 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
- recurrent neural circuits, persistent neuronal activity, synaptic potentiation, short-term memory, Drosophila, memory encoding
- MeSH terms
- Animals, Courtship, Drosophila, Memory, Models, Neurological, Neural Pathways, Mushroom Bodies, Dopaminergic Neurons
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