Excitatory Local Circuits and Their Implications for Olfactory Processing in the Fly Antennal Lobe
Open accessAbstract
Conflicting views exist of how circuits of the antennal lobe, the insect equivalent of the olfactory bulb, translate input from olfactory receptor neurons (ORNs) into projection-neuron (PN) output. Synaptic connections between ORNs and PNs are one-to-one, yet PNs are more broadly tuned to odors than ORNs. The basis for this difference in receptive range remains unknown. Analyzing a Drosophila mutant lacking ORN input to one glomerulus, we show that some of the apparent complexity in the antennal lobe's output arises from lateral, interglomerular excitation of PNs. We describe a previously unidentified population of cholinergic local neurons (LNs) with multiglomerular processes. These excitatory LNs respond broadly to odors but exhibit little glomerular specificity in their synaptic output, suggesting that PNs are driven by a combination of glomerulus-specific ORN afferents and diffuse LN excitation. Lateral excitation may boost PN signals and enhance their transmission to third-order neurons in a mechanism akin to stochastic resonance.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Literature expected perhaps as many as approximately 15 cholinergic local neurons.
“We also expected perhaps as many as ∼ 15 cholinergic local neurons.63,189”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [63]
Among the lLN2T_abc neurons are approximately 13 neurons that have a cell body placement and general morphology most similar to reported cholinergic local neurons.
“Specifically, among them are ∼ 13 lLN2T_abc neurons that have a cell body placement and general morphology most similar to reported cholinergic local neurons.63,189”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [63]
The predicted cholinergic local neurons in 'ALl1 dorsal' are unilateral and pan-glomerular, in accordance with previous descriptions but more numerous.
“The predicted cholinergic neurons are unilateral and ‘broad’, i.e., pan-glomerular, in accordance with previous descriptions63,189 but more numerous.”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [63]
Antennal lobe local neurons are known to express acetylcholine, GABA, glutamate and various neuropeptides.
“They are known to express acetylcholine,63,189,190 GABA,62,89,151 glutamate61,89,104 and various neuropeptides transmitters.106”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [63]
The remainder of the lLN2T_abc neurons is most likely GABAergic, e.g., lLN2_d gross morphology looks more like related GABAergic neurons.
“The remainder is most likely GABAergic, e.g., lLN2_d gross morphology looks more like related GABAergic neurons.63,189”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [63]
Cites
Gammaitoni, L., Hänggi, P., Jung, P., & Marchesoni, F. (1998) · Reviews of Modern Physics · doi:10.1103/revmodphys.70.223 · Cited by 5,443 · see citing works
A novel multigene family may encode odorant receptors: A molecular basis for odor recognition
Buck, L., & Axel, R. (1991) · Cell · doi:10.1016/0092-8674(91)90418-x · Cited by 4,987 · see citing works
Spatial registration and normalization of images
Friston, K. J., Ashburner, J., Frith, C., Poline, J.-B., Heather, J. D., & Frackowiak, R. S. J. (1995) · Human Brain Mapping · doi:10.1002/hbm.460030303 · Cited by 3,744 · see citing works
Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins
Miesenböck, G., Angelis, D. A. D., & Rothman, J. E. (1998) · Nature · doi:10.1038/28190 · Cited by 2,569 · see citing works
Self-citationLee, T., & Luo, L. (1999) · Neuron · doi:10.1016/s0896-6273(00)80701-1 · Cited by 2,540 · see citing works
Visualizing an Olfactory Sensory Map
Mombaerts, P., Wang, F., Dulac, C. G., Chao, S. K., Nemes, A., Mendelsohn, M. M., Edmondson, J., & Axel, R. (1996) · Cell · doi:10.1016/s0092-8674(00)81387-2 · Cited by 1,992 · see citing works
Stochastic resonance and the benefits of noise: from ice ages to crayfish and SQUIDs
Wiesenfeld, K., & Moss, F. (1995) · Nature · doi:10.1038/373033a0 · Cited by 1,830 · see citing works
Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance
Douglass, J. K., Wilkens, L. A., Pantazelou, E., & Moss, F. (1993) · Nature · doi:10.1038/365337a0 · Cited by 1,433 · 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
Topographic organization of sensory projections to the olfactory bulb
Vassar, R. J., Chao, S. K., Sitcheran, R., ̃ez, J. M. N., Vosshall, L. B., & Axel, R. (1994) · Cell · doi:10.1016/0092-8674(94)90029-9 · Cited by 1,281 · see citing works
Coding of Odors by a Receptor Repertoire
Hallem, E. A., & Carlson, J. R. (2006) · Cell · doi:10.1016/j.cell.2006.01.050 · Cited by 1,265 · see citing works
Ressler, K. J., Sullivan, S. L., & Buck, L. B. (1994) · Cell · doi:10.1016/0092-8674(94)90015-9 · Cited by 1,202 · see citing works
A Spatial Map of Olfactory Receptor Expression in the Drosophila Antenna
Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A., & Axel, R. (1999) · Cell · doi:10.1016/s0092-8674(00)80582-6 · Cited by 1,166 · see citing works
A Novel Family of Divergent Seven-Transmembrane Proteins
Clyne, P. J., Warr, C. G., Freeman, M. R., Lessing, D., Kim, J., & Carlson, J. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)81093-4 · Cited by 1,155 · see citing works
An Olfactory Sensory Map in the Fly Brain
Vosshall, L. B., Wong, A. M., & Axel, R. (2000) · Cell · doi:10.1016/s0092-8674(00)00021-0 · Cited by 1,090 · see citing works
The Molecular Basis of Odor Coding in the Drosophila Antenna
Hallem, E. A., Ho, M. G.-R., & Carlson, J. R. (2004) · Cell · doi:10.1016/j.cell.2004.05.012 · Cited by 993 · see citing works
Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System
Couto, A., Alenius, M., & Dickson, B. J. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.034 · Cited by 967 · see citing works
Kitamoto, T. (2001) · Journal of Neurobiology · doi:10.1002/neu.1018 · Cited by 868 · see citing works
Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain
Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B., & Axel, R. (2003) · Cell · doi:10.1016/s0092-8674(03)00004-7 · Cited by 801 · see citing works
Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears
Zheng, J. L., & Gao, W. (2000) · Nature Neuroscience · doi:10.1038/75753 · Cited by 797 · see citing works
Oscillations and Sparsening of Odor Representations in the Mushroom Body
Pérez-Orive, J., Mazor, O., Turner, G. C., Cassenaer, S., Wilson, R. I., & Laurent, G. (2002) · Science · doi:10.1126/science.1070502 · Cited by 792 · see citing works
Dynamics of Encoding in a Population of Neurons
Knight, B. W. (1972) · The Journal of General Physiology · doi:10.1085/jgp.59.6.734 · Cited by 720 · see citing works
Broadband neural encoding in the cricket cereal sensory system enhanced by stochastic resonance
Levin, J. E., & Miller, J. P. (1996) · Nature · doi:10.1038/380165a0 · Cited by 677 · see citing works
Intensity versus identity coding in an olfactory system.
Stopfer, M., Jayaraman, V., & Laurent, G. (2003) · Neuron · doi:10.1016/j.neuron.2003.08.011 · Cited by 627 · see citing works
Genetic and Functional Subdivision of the Drosophila Antennal Lobe
Fishilevich, E., & Vosshall, L. B. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.066 · Cited by 608 · see citing works
Remote Control of Behavior through Genetically Targeted Photostimulation of Neurons
Lima, S. Q., & Miesenböck, G. (2005) · Cell · doi:10.1016/j.cell.2005.02.004 · Cited by 562 · see citing works
Self-citationIntegrating the Molecular and Cellular Basis of Odor Coding in the Drosophila Antenna
Dobritsa, A. A., van Naters, W. V. D. G., Warr, C. G., Steinbrecht, R. A., & Carlson, J. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00094-1 · Cited by 555 · see citing works
Transformation of Olfactory Representations in the Drosophila Antennal Lobe
Wilson, R. I., Turner, G. C., & Laurent, G. (2003) · Science · doi:10.1126/science.1090782 · Cited by 554 · see citing works
Longtin, A., Bulsara, A. R., & Moss, F. (1991) · Physical Review Letters · doi:10.1103/physrevlett.67.656 · Cited by 512 · see citing works
Improving structural integrity of cryosections for immunogold labeling
Liou, W., Geuze, H. J., & Slot, J. W. (1996) · Histochemistry and Cell Biology · doi:10.1007/bf02473201 · Cited by 507 · see citing works
Identification of Candidate Drosophila Olfactory Receptors from Genomic DNA Sequence
Gao, Q., & Chess, A. J. (1999) · Genomics · doi:10.1006/geno.1999.5894 · Cited by 495 · see citing works
Mazor, O., & Laurent, G. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.032 · Cited by 484 · see citing works
Wilson, R. I., & Laurent, G. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2070-05.2005 · Cited by 475 · see citing works
Ng, M., Roorda, R. D., Lima, S. Q., Zemelman, B. V., Morcillo, P., & Miesenböck, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00975-3 · Cited by 475 · see citing works
Self-citationNeuronal architecture of the antennal lobe in Drosophila melanogaster
Stocker, R. F., Lienhard, M. C., Borst, A., & Fischbach, K. F. (1990) · Cell and Tissue Research · doi:10.1007/bf00327741 · Cited by 457 · see citing works
The 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
Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe
Gao, Q., Yuan, B., & Chess, A. J. (2000) · Nature Neuroscience · doi:10.1038/77680 · Cited by 432 · see citing works
Target neuron prespecification in the olfactory map of Drosophila
Jefferis, G. S. X. E., Marin, E. C., Stocker, R. F., & Luo, L. (2001) · Nature · doi:10.1038/35102574 · Cited by 418 · see citing works
Cell Killing by the Drosophila Gene reaper
White, K., Tahaoglu, E., & Steller, H. (1996) · Science · doi:10.1126/science.271.5250.805 · Cited by 387 · see citing works
Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster
Neuhaus, E. M., Gisselmann, G., Zhang, W., Dooley, R., Störtkuhl, K. F., & Hatt, H. H. (2004) · Nature Neuroscience · doi:10.1038/nn1371 · Cited by 339 · see citing works
Odorant-induced oscillations in the mushroom bodies of the locust
Laurent, G., & Naraghi, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02993.1994 · Cited by 286 · see citing works
Glutamate Spillover Mediates Excitatory Transmission in the Rat Olfactory Bulb
Isaacson, J. S. (1999) · Neuron · doi:10.1016/s0896-6273(00)80787-4 · Cited by 229 · see citing works
Lateral Interactions in Primary Visual Cortex: A Model Bridging Physiology and Psychophysics
Stemmler, M., Usher, M., & Niebur, E. (1995) · Science · doi:10.1126/science.7569930 · Cited by 225 · see citing works
Stochastic Resonance: From Suprathreshold Stochastic Resonance to Stochastic Signal Quantization
McDonnell, M. D., Stocks, N. G., Pearce, C. E. M., & Abbott, D. (2009) · Adelaide Research & Scholarship (AR&S) (University of Adelaide) · doi:10.1017/cbo9780511535239 · Cited by 212 · see citing works
Wang, Y., Guo, H.-F., Pologruto, T. A., Hannan, F., Hakker, I., Svoboda, K., & Zhong, Y. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3727-03.2004 · Cited by 195 · see citing works
AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli
Schoppa, N. E., & Westbrook, G. L. (2002) · Nature Neuroscience · doi:10.1038/nn953 · Cited by 178 · see citing works
Intrinsic and Circuit Properties Favor Coincidence Detection for Decoding Oscillatory Input
Pérez-Orive, J., Bazhenov, M., & Laurent, G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1084-04.2004 · Cited by 124 · see citing works
Komiyama, T., Carlson, J. R., & Luo, L. (2004) · Nature Neuroscience · doi:10.1038/nn1284 · Cited by 106 · see citing works
Wiring Stability of the AdultDrosophilaOlfactory Circuit after Lesion
Berdnik, D., Chihara, T., Couto, A., & Luo, L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4941-05.2006 · Cited by 98 · see citing works
Video-Rate Nonlinear Microscopy of Neuronal Membrane Dynamics With Genetically Encoded Probes
Roorda, R. D., Hohl, T. M., Toledo‐Crow, R., & Miesenböck, G. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00087.2004 · Cited by 72 · see citing works
Self-citationBuchner, E. (1991) · Journal of Neurogenetics · doi:10.3109/01677069109167432 · Cited by 69 · see citing works
Takagawa, K., & Salvaterra, P. M. (1996) · Neuroscience Research · doi:10.1016/0168-0102(95)00999-x · Cited by 64 · 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
Buonviso, N., Chaput, M. A., & Scott, J. W. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903070106 · Cited by 51 · see citing works
Computation of olfactory signals inDrosophila melanogaster
Borst, A. (1983) · Journal of Comparative Physiology A · doi:10.1007/bf00606242 · Cited by 47 · see citing works
Kitamoto, T., Ikeda, K., & Salvaterra, P. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-05-01628.1992 · Cited by 43 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dephasing-assisted transport: quantum networks and biomolecules
Plenio, M. B., & Huelga, S. F. (2008) · New Journal of Physics · doi:10.1088/1367-2630/10/11/113019 · Cited by 1,002 · see citing works
Molecular Architecture of Smell and Taste in Drosophila
Vosshall, L. B., & Stocker, R. F. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094306 · Cited by 860 · see citing works
The benefits of noise in neural systems: bridging theory and experiment
McDonnell, M. D., & Ward, L. M. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3061 · Cited by 763 · 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
Olfactory Perception: Receptors, Cells, and Circuits
Su, C., Menuz, K., & Carlson, J. R. (2009) · Cell · doi:10.1016/j.cell.2009.09.015 · Cited by 577 · see citing works
Lateral presynaptic inhibition mediates gain control in an olfactory circuit
Olsen, S. R., & Wilson, R. I. (2008) · Nature · doi:10.1038/nature06864 · Cited by 549 · 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
Divisive Normalization in Olfactory Population Codes
Olsen, S. R., Bhandawat, V., & Wilson, R. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.009 · Cited by 500 · see citing works
Silbering, A. F., Rytz, R., Grosjean, Y., Abuin, L., Ramdya, P. P., Jefferis, G. S. X. E., & Benton, R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2360-11.2011 · Cited by 486 · see citing works
Olfactory Representations by Drosophila Mushroom Body Neurons
Turner, G. C., Bazhenov, M., & Laurent, G. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01283.2007 · Cited by 416 · see citing works
Early Olfactory Processing in <i>Drosophila</i>: Mechanisms and Principles
Wilson, R. I. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150533 · Cited by 394 · 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
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
Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe
Chou, Y.-H., Spletter, M. L., Yaksi, E., Leong, J. C. S., Wilson, R. I., & Luo, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2489 · Cited by 361 · see citing works
Select Drosophila glomeruli mediate innate olfactory attraction and aversion
Semmelhack, J. L., & Wang, J. W. (2009) · Nature · doi:10.1038/nature07983 · Cited by 360 · see citing works
Bhandawat, V., Olsen, S. R., Gouwens, N. W., Schlief, M. L., & Wilson, R. I. (2007) · Nature Neuroscience · doi:10.1038/nn1976 · Cited by 354 · see citing works
A Presynaptic Gain Control Mechanism Fine-Tunes Olfactory Behavior
Root, C. M., Masuyama, K., Green, D. S., Enell, L. E., Nässel, D. R., Lee, C., & Wang, J. W. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.003 · Cited by 352 · see citing works
Glutamate is an inhibitory neurotransmitter in the <i>Drosophila</i> olfactory system
Liu, W. W., & Wilson, R. I. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220560110 · Cited by 297 · see citing works
Olfactory Information Processing in Drosophila
Masse, N. Y., Turner, G. C., & Jefferis, G. S. X. E. (2009) · Current Biology · doi:10.1016/j.cub.2009.06.026 · Cited by 329 · 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
Self-citationExcitatory Interactions between Olfactory Processing Channels in the Drosophila Antennal Lobe
Olsen, S. R., Bhandawat, V., & Wilson, R. I. (2007) · Neuron · doi:10.1016/j.neuron.2007.03.010 · Cited by 291 · see citing works
Translation of Sensory Input into Behavioral Output via an Olfactory System
Kreher, S. A., Mathew, D., Kim, J., & Carlson, J. R. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.010 · Cited by 263 · see citing works
Genetically Targeted Optical Electrophysiology in Intact Neural Circuits
Cao, G., Platiša, J., Pieribone, V. A., Raccuglia, D., Kunst, M., & Nitabach, M. N. (2013) · Cell · doi:10.1016/j.cell.2013.07.027 · Cited by 262 · see citing works
Miesenböck, G. (2009) · Science · doi:10.1126/science.1174520 · Cited by 255 · see citing works
Self-citationBathellier, B., Buhl, D. L., Accolla, R., & Carleton, A. (2008) · Neuron · doi:10.1016/j.neuron.2008.02.011 · Cited by 254 · 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
The neurobiology of insect olfaction: Sensory processing in a comparative context
Martin, J. P., Beyerlein, A., Dacks, A. M., Reisenman, C. E., Riffell, J. A., Lei, H., & Hildebrand, J. G. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.09.007 · Cited by 225 · see citing works
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
Activity-Dependent Plasticity in an Olfactory Circuit
Sachse, S., Rueckert, E. H., Keller, A., Okada, R., Tanaka, N. K., Ito, K., & Vosshall, L. B. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.035 · Cited by 219 · see citing works
Silbering, A. F., & Galizia, C. G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3099-07.2007 · Cited by 218 · see citing works
Integration of Parallel Opposing Memories Underlies Memory Extinction
Felsenberg, J., Jacob, P. F., Walker, T. M., Barnstedt, O., Edmondson-Stait, A. J., Pleijzier, M. W., Otto, N., Schlegel, P., Sharifi, N., Perisse, E., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.021 · Cited by 217 · see citing works
The Color-Vision Circuit in the Medulla of Drosophila
Morante, J., & Desplan, C. (2008) · Current Biology · doi:10.1016/j.cub.2008.02.075 · Cited by 215 · see citing works
Insect olfaction from model systems to disease control
Carey, A. F., & Carlson, J. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103472108 · Cited by 208 · 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
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
Electrical Coupling between Olfactory Glomeruli
Yaksi, E., & Wilson, R. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.041 · Cited by 190 · see citing works
Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila
Ignell, R., Root, C. M., Birse, R. T., Wang, J. W., Nässel, D. R., & Winther, Å. M. E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813004106 · Cited by 193 · see citing works
Homeostatic Matching and Nonlinear Amplification at Identified Central Synapses
Kazama, H., & Wilson, R. I. (2008) · Neuron · doi:10.1016/j.neuron.2008.02.030 · Cited by 190 · see citing works
Elucidating the Neuronal Architecture of Olfactory Glomeruli in the Drosophila Antennal Lobe
Grabe, V., Baschwitz, A., Dweck, H. K. M., Lavista-Llanos, S., Hansson, B. S., & Sachse, S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.08.063 · Cited by 186 · see citing works
Neural Circuit Mechanisms for Pattern Detection and Feature Combination in Olfactory Cortex
Davison, I. G., & Ehlers, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.047 · Cited by 179 · see citing works
Dissecting functional connectivity of neuronal microcircuits: experimental and theoretical insights
Muldoon, S. F., Bonifazi, P., & Cossart, R. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.02.007 · Cited by 177 · see citing works
Information flow, cell types and stereotypy in a full olfactory connectome
Schlegel, P., Bates, A. S., Stürner, T., Jagannathan, S. R., Drummond, N., Hsu, J., Serratosa Capdevila, L., Javier, A., Marin, E. C., Barth-Maron, A., et al. (2021) · eLife · doi:10.7554/elife.66018 · Cited by 178 · see citing works
Hendel, T., Mank, M., Schnell, B., Griesbeck, O., Borst, A., & Reiff, D. F. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1038-08.2008 · Cited by 174 · see citing works
Lai, S.-L., Awasaki, T., Ito, K., & Lee, T. (2008) · Development · doi:10.1242/dev.024380 · Cited by 171 · see citing works
Flying the Fly: Long-range Flight Behavior of Drosophila melanogaster to Attractive Odors
Becher, P. G., Bengtsson, M., Hansson, B. S., & Witzgall, P. (2010) · Journal of Chemical Ecology · doi:10.1007/s10886-010-9794-2 · Cited by 170 · see citing works
Odor Information Processing by the Olfactory Bulb Analyzed in Gene-Targeted Mice
Tan, J., Savigner, A., Ma, M., & Luo, M. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.011 · Cited by 170 · see citing works
Organization of antennal lobe‐associated neurons in adult Drosophila melanogaster brain
Tanaka, N. K., Endo, K., & Ito, K. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23142 · Cited by 168 · see citing works
Testing Odor Response Stereotypy in the Drosophila Mushroom Body
Murthy, M., Fiete, I., & Laurent, G. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.040 · Cited by 163 · 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
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
A circuit supporting concentration-invariant odor perception in Drosophila
Asahina, K., Louis, M., Piccinotti, S., & Vosshall, L. B. (2009) · Journal of Biology · doi:10.1186/jbiol108 · Cited by 156 · see citing works
Rapid odor processing in the honeybee antennal lobe network
Krofczik, S. (2008) · Frontiers in Computational Neuroscience · doi:10.3389/neuro.10.009.2008 · Cited by 151 · see citing works
Olfactory coding in the insect brain: data and conjectures
Galizia, C. G. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12558 · Cited by 151 · see citing works
GABAA Receptor RDL Inhibits Drosophila Olfactory Associative Learning
Liu, X., Krause, W. C., & Davis, R. L. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.036 · Cited by 151 · see citing works
Huang, J., Zhang, W., Qiao, W., Hu, A., & Wang, Z. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.025 · Cited by 148 · see citing works
Seki, Y., Rybak, J., Wicher, D., Sachse, S., & Hansson, B. S. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00249.2010 · Cited by 147 · see citing works
Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons
Thorne, N., & Amrein, H. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21547 · Cited by 147 · see citing works
Gamma‐aminobutyric acid (GABA)‐mediated neural connections in the <i>Drosophila</i> antennal lobe
Okada, R., Awasaki, T., & Ito, K. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21971 · Cited by 146 · see citing works
Multiple neuropeptides in the <i>Drosophila</i> antennal lobe suggest complex modulatory circuits
Carlsson, M. A., Diesner, M., Schachtner, J., & Nässel, D. R. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22405 · Cited by 146 · see citing works
Generating sparse and selective third-order responses in the olfactory system of the fly
Luo, S. X., Axel, R., & Abbott, L. F. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005635107 · Cited by 139 · see citing works
Olfactory processing and behavior downstream from highly selective receptor neurons
Schlief, M. L., & Wilson, R. I. (2007) · Nature Neuroscience · doi:10.1038/nn1881 · Cited by 143 · see citing works
Olsen, S. R., & Wilson, R. I. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.07.006 · Cited by 138 · see citing works
Fundamental principles of the olfactory code
Grabe, V., & Sachse, S. (2017) · Biosystems · doi:10.1016/j.biosystems.2017.10.010 · Cited by 140 · see citing works
Odor-Evoked Neural Oscillations in Drosophila Are Mediated by Widely Branching Interneurons
Tanaka, N. K., Ito, K., & Stopfer, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1455-09.2009 · Cited by 133 · see citing works
Olfactory Information Processing in theDrosophilaAntennal Lobe: Anything Goes?
Silbering, A. F., Okada, R., Ito, K., & Galizia, C. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2973-08.2008 · Cited by 131 · see citing works
Propagation of olfactory information in Drosophila
Root, C. M., Semmelhack, J. L., Wong, A. M., Flores, J., & Wang, J. W. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704523104 · Cited by 129 · see citing works
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 · see citing works
Single-cell transcriptomes of developing and adult olfactory receptor neurons in Drosophila
McLaughlin, C. N., Brbić, M., Xie, Q., Li, T., Horns, F., Kolluru, S. S., Kebschull, J. M., Vacek, D., Xie, A., Li, J., et al. (2021) · eLife · doi:10.7554/elife.63856 · Cited by 111 · see citing works
Serotonin Modulates Olfactory Processing in the Antennal Lobe ofDrosophila
Dacks, A. M., Green, D. S., Root, C. M., Nighorn, A. J., & Wang, J. W. (2009) · Journal of Neurogenetics · doi:10.3109/01677060903085722 · Cited by 117 · see citing works
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila
Jacob, P. F., & Waddell, S. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.013 · Cited by 112 · see citing works
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 · see citing works
State of the Art on Insect Nicotinic Acetylcholine Receptor Function in Learning and Memory
Gauthier, M. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6445-8_9 · Cited by 109 · see citing works
Functional and anatomical specificity in a higher olfactory centre
Frechter, S., Bates, A. S., Tootoonian, S., Dolan, M.-J., Manton, J., Jamasb, A. R., Kohl, J., Bock, D., & Jefferis, G. (2019) · eLife · doi:10.7554/elife.44590 · Cited by 105 · see citing works
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 103 · see citing works
Decoding of Context-Dependent Olfactory Behavior in Drosophila
Badel, L., Ohta, K., Tsuchimoto, Y., & Kazama, H. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.022 · Cited by 100 · see citing works
Ghaninia, M., Ignell, R., & Hansson, B. S. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05786.x · Cited by 93 · see citing works
Dupuis, J. P., Louis, T., Gauthier, M., & Raymond, V. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.04.003 · Cited by 91 · see citing works
Topological Reorganization of Odor Representations in the Olfactory Bulb
Yaksi, E., Judkewitz, B., & Friedrich, R. W. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050178 · Cited by 91 · see citing works
Multiple memory traces after associative learning in the honey bee antennal lobe
Rath, L., Galizia, C. G., & Szyszka, P. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07753.x · Cited by 87 · see citing works
Central Processing of Natural Odor Mixtures in Insects
Lei, H., & Vickers, N. J. (2008) · Journal of Chemical Ecology · doi:10.1007/s10886-008-9487-2 · Cited by 82 · see citing works
Metamorphosis of an identified serotonergic neuron in the Drosophila olfactory system
Roy, B., Singh, A. P., Shetty, C., Chaudhary, V., North, A., Landgraf, M., VijayRaghavan, K., & Rodrigues, V. (2007) · Neural Development · doi:10.1186/1749-8104-2-20 · Cited by 84 · see citing works
Peripheral modulation of pheromone response by inhibitory host compound in a beetle
Andersson, M. N., Larsson, M. C., Blaženec, M., Jakuš, R., Zhang, Q., & Schlyter, F. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.044396 · Cited by 81 · see citing works
Shocking Revelations and Saccharin Sweetness in the Study of Drosophila Olfactory Memory
Perisse, E., Burke, C., Huetteroth, W., & Waddell, S. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.060 · Cited by 76 · see citing works
Dendritic Integration of Sensory Evidence in Perceptual Decision-Making
Groschner, L. N., Hak, L. C. W., Bogacz, R., Dasgupta, S., & Miesenböck, G. (2018) · Cell · doi:10.1016/j.cell.2018.03.075 · Cited by 77 · see citing works
Self-citationFunctional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway
Hu, A., Zhang, W., & Wang, Z. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914912107 · Cited by 76 · see citing works
Lin, S., Lai, S.-L., Yu, H., Chihara, T., Luo, L., & Lee, T. (2009) · Development · doi:10.1242/dev.041699 · Cited by 74 · see citing works
Mechanisms of odor-tracking: multiple sensors for enhanced perception and behavior
Gómez-Marín, À. (2010) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2010.00006 · Cited by 74 · see citing works
Pheromone processing in Drosophila
Kohl, J., Huoviala, P., & Jefferis, G. S. X. E. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.06.009 · Cited by 74 · see citing works
Das, A., Sen, S., Lichtneckert, R., Okada, R., Ito, K., Rodrigues, V., & Reichert, H. (2008) · Neural Development · doi:10.1186/1749-8104-3-33 · Cited by 73 · see citing works
Sensitivity and specificity in Drosophila pheromone perception
Benton, R. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.07.004 · Cited by 73 · see citing works
RETRACTED ARTICLE: Multisensory learning binds neurons into a cross-modal memory engram
Okray, Z., Jacob, P. F., Stern, C., Desmond, K., Otto, N., Talbot, C. B., Vargas-Gutierrez, P., & Waddell, S. (2023) · Nature · doi:10.1038/s41586-023-06013-8 · Cited by 78 · see citing works
RetractedNamiki, S., Iwabuchi, S., & Kanzaki, R. (2008) · Journal of Comparative Physiology A · doi:10.1007/s00359-008-0325-3 · Cited by 69 · see citing works
DSL-Notch Signaling in the Drosophila Brain in Response to Olfactory Stimulation
Lieber, T., Kidd, S., & Struhl, G. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.015 · Cited by 69 · see citing works
Namiki, S. (2008) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.001.2008 · Cited by 68 · see citing works
Neonicotinoid-induced impairment of odour coding in the honeybee
Andrione, M., Vallortígara, G., Antolini, R., & Haase, A. (2016) · Scientific Reports · doi:10.1038/srep38110 · Cited by 63 · see citing works
Localized olfactory representation in mushroom bodies of Drosophila larvae
Masuda-Nakagawa, L. M., Gendre, N., O’Kane, C. J., & Stocker, R. F. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900178106 · Cited by 64 · see citing works
Tantama, M., Hung, Y. P., & Yellen, G. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59426-6.00012-4 · Cited by 62 · see citing works
Innate Attractiveness and Associative Learnability of Odors Can Be Dissociated in Larval Drosophila
Saumweber, T., Husse, J., & Gerber, B. (2011) · Chemical Senses · doi:10.1093/chemse/bjq128 · Cited by 62 · see citing works
Mechanisms of translational regulation by a human eIF5-mimic protein
Singh, C. R., Watanabe, R., Zhou, D., Jennings, M. D., Fukao, A., Lee, B., Ikeda, Y., Chiorini, J. A., Campbell, S. G., Ashe, M., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr339 · Cited by 60 · see citing works
Jayaraman, V. (2007) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.003.2007 · Cited by 60 · see citing works
- Authors
- Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M., & Miesenböck, G.
- Affiliations
- Yale University (US)
- Corresponding author
- Miesenböck, Gero
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2007-02
- Volume
- 128
- Issue
- 3
- Pages
- 601-612
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC2866183
- OpenAlex
- W2073936984
- Cited by
- 359
- References
- 56
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 15 · 2023: 19 · 2022: 7 · 2021: 24 · 2020: 10 · 2019: 13 · 2018: 8 · 2017: 11 · 2016: 16 · 2015: 16 · 2014: 21 · 2013: 15 · 2012: 25
- FWCI
- 16.32
- 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, 2358 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)
- Funders
- National Institute on Deafness and Other Communication Disorders (R01DC005810)
- 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 › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- antennal lobe, olfactory processing, Drosophila, olfactory sensory neurons, projection neurons, local circuits, stochastic resonance
- MeSH terms
- Acetylcholine, Animals, Brain, Drosophila, Nerve Net, Neurons, Afferent, Odorants, Smell, Synapses, Olfactory Receptor Neurons, Receptors, Odorant, 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