Early Olfactory Processing in Drosophila: Mechanisms and Principles
Open accessAbstract
In the olfactory system of Drosophila melanogaster, it is relatively straightforward to target in vivo measurements of neural activity to specific processing channels. This, together with the numerical simplicity of the Drosophila olfactory system, has produced rapid gains in our understanding of Drosophila olfaction. This review summarizes the neurophysiology of the first two layers of this system: the peripheral olfactory receptor neurons and their postsynaptic targets in the antennal lobe. We now understand in some detail the cellular and synaptic mechanisms that shape odor representations in these neurons. Together, these mechanisms imply that interesting neural adaptations to environmental statistics have occurred. These mechanisms also place some fundamental constraints on early sensory processing that pose challenges for higher brain regions. These findings suggest some general principles with broad relevance to early sensory processing in other modalities.
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?
These resources and tools have led to the emergence of data-constrained models of neural circuits.
“These resources and tools have led to the emergence of data-constrained models of neural circuits (e.g., 43,44 ).”
From NeuroMechFly v2: simulating embodied sensorimotor control in adult Drosophila (2024) · cites this paper as [44]
The Introduction describes recording and genetic tools that transformed Drosophila neurophysiology, and “Some Fundamental Principles” discusses simulations of olfactory-circuit processing. The passages do not establish that those tools led to the emergence of data-constrained neural-circuit models specifically. (LLM, conf=0.76)
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
Normalization as a canonical neural computation
Carandini, M., & Heeger, D. J. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3136 · Cited by 1,906 · see citing works
The organization of the chemosensory system in Drosophila melanogaster: a rewiew
Stocker, R. F. (1994) · Cell and Tissue Research · doi:10.1007/bf00305372 · Cited by 950 · 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
Self-citationExcitatory Local Circuits and Their Implications for Olfactory Processing in the Fly Antennal Lobe
Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M., & Miesenböck, G. (2007) · Cell · doi:10.1016/j.cell.2006.12.034 · Cited by 359 · see citing works
A dimorphic pheromone circuit in Drosophila from sensory input to descending output
Ruta, V., Datta, S. R., Vasconcelos, M. L., Freeland, J., Looger, L. L., & Axel, R. (2010) · Nature · doi:10.1038/nature09554 · Cited by 344 · 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
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
Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila
Gaudry, Q., Hong, E. J., Kain, J., de Bivort, B. L., & Wilson, R. I. (2013) · Nature · doi:10.1038/nature11747 · Cited by 146 · see citing works
Self-citationMultiple 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
Das, A., Chiang, A., Davla, S., Priya, R., Reichert, H., VijayRaghavan, K., & Rodrigues, V. (2011) · Neural Systems & Circuits · doi:10.1186/2042-1001-1-4 · Cited by 38 · see citing works
Flagged first, then by citations
Research works printed but not linked: 134
- Abbott LF 2008 Theoretical neuroscience rising Neuron 60 489 95 18995824
- Abbott LF Varela JA Sen K Nelson SB 1997 Synaptic depression and cortical gain control Science 275 220 24 8985017
- Abuin L Bargeton B Ulbrich MH Isacoff EY Kellenberger S Benton R 2011 Functional architecture of olfactory ionotropic glutamate receptors Neuron 69 44 60 21220098 PMC3050028
- Asahina K Louis M Piccinotti S Vosshall LB 2009 A circuit supporting concentration-invariant odor perception in Drosophila J Biol 8 9 19171076 PMC2656214
- Baines RA Bate M 1998 Electrophysiological development of central neurons in the Drosophila embryo J Neurosci 18 4673 83 9614242 PMC6792699
- Bargmann CI 2006 Comparative chemosensation from receptors to ecology Nature 444 295 301 17108953
- Benton R Sachse S Michnick SW Vosshall LB 2006 Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo PLoS Biol 4 e20 16402857 PMC1334387
- Benton R Vannice KS Gomez-Diaz C Vosshall LB 2009 Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila Cell 136 149 62 19135896 PMC2709536
- Bhandawat V Maimon G Dickinson MH Wilson RI 2010 Olfactory modulation of flight in Drosophila is sensitive, selective and rapid J Exp Biol 213 3625 35 20952610 PMC2956223
- Bhandawat V Olsen SR Schlief ML Gouwens NW Wilson RI 2007 Sensory processing in the Drosophila antennal lobe increases the reliability and separability of ensemble odor representations Nat Neurosci 10 1474 82 17922008 PMC2838615
- Bhandawat V Reisert J Yau KW 2005 Elementary response of olfactory receptor neurons to odorants Science 308 1931 34 15976304 PMC2957801
- Borst A 2007 The broader, the better? Drosophila olfactory interneurons are found to respond to a wider range of odorants than their immediate sensory input Neuron 54 6 8 17408571
- Brand AH Perrimon N 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Development 118 401 15 8223268
- Brochtrup A Hummel T 2011 Olfactory map formation in the Drosophila brain: genetic specificity and neuronal variability Curr Opin Neurobiol 21 85 92 21112768
- Choi JC Park D Griffith LC 2004 Electrophysiological and morphological characterization of identified motor neurons in the Drosophila third instar larva central nervous system J Neurophysiol 91 2353 65 14695352
- Chou YH Spletter ML Yaksi E Leong JC Wilson RI Luo L 2010 Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe Nat Neurosci 13 439 49 20139975 PMC2847188
- Christie JM Westbrook GL 2006 Lateral excitation within the olfactory bulb J Neurosci 26 2269 77 16495454 PMC6674816
- Cleland TA 2010 Early transformations in odor representation Trends Neurosci 33 130 39 20060600 PMC2839009
- Clyne P Grant A O’Connell R Carlson JR 1997 Odorant response of individual sensilla on the Drosophila antenna Invertebr Neurosci 3 127 35 9783438
- Couto A Alenius M Dickson BJ 2005 Molecular, anatomical, and functional organization of the Drosophila olfactory system Curr Biol 15 1535 47 16139208
- Dacks AM Green DS Root CM Nighorn AJ Wang JW 2009 Serotonin modulates olfactory processing in the antennal lobe of Drosophila J Neurogenet 23 366 77 19863268 PMC2850205
- Daniels RW Gelfand MV Collins CA DiAntonio A 2008 Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS J Comp Neurol 508 131 52 18302156
- Das A Sen S Lichtneckert R Okada R Ito K 2008 Drosophila olfactory local interneurons and projection neurons derive from a common neuroblast lineage specified by the empty spiracles gene Neural Dev 3 33 19055770 PMC2647541
- Datta SR Vasconcelos ML Ruta V Luo S Wong A 2008 The Drosophila pheromone cVA activates a sexually dimorphic neural circuit Nature 452 473 77 18305480
- de Bruyne M Clyne PJ Carlson JR 1999 Odor coding in a model olfactory organ: the Drosophila maxillary palp J Neurosci 19 4520 32 10341252 PMC6782632
- de Bruyne M Foster K Carlson JR 2001 Odor coding in the Drosophila antenna Neuron 30 537 52 11395013
- Dekker T Carde RT 2011 Moment-to-moment flight manoeuvres of the female yellow fever mosquito (Aedes aegypti L.) in response to plumes of carbon dioxide and human skin odour J Exp Biol 214 3480 94 21957112
- Dekker T Ibba I Siju KP Stensmyr MC Hansson BS 2006 Olfactory shifts parallel superspecialism for toxic fruit in Drosophilamelanogaster sibling, D. sechellia Curr Biol 16 101 9 16401429
- Deshpande M Venkatesh K Rodrigues V Hasan G 2000 The inositol 1,4,5-trisphosphate receptor is required for maintenance of olfactory adaptation in Drosophila antennae J Neurobiol 43 282 88 10842240
- Dhawale AK Hagiwara A Bhalla US Murthy VN Albeanu DF 2010 Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse Nat Neurosci 13 1404 12 20953197 PMC3208311
- Dobritsa AA van der Goes van Naters W Warr CG Steinbrecht RA Carlson JR 2003 Integrating the molecular and cellular basis of odor coding in the Drosophila antenna Neuron 37 827 41 12628173
- Duistermars BJ Chow DM Frye MA 2009 Flies require bilateral sensory input to track odor gradients in flight Curr Biol 19 1301 7 19576769 PMC2726901
- Eisthen HL 2002 Why are olfactory systems of different animals so similar? Brain Behav Evol 59 273 93 12207084
- Elmore T Ignell R Carlson JR Smith DP 2003 Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum J Neurosci 23 9906 12 14586020 PMC6740877
- Fantana AL Soucy ER Meister M 2008 Rat olfactory bulb mitral cells receive sparse glomerular inputs Neuron 59 802 14 18786363
- Field GD Sampath AP Rieke F 2005 Retinal processing near absolute threshold: from behavior to mechanism Annu Rev Physiol 67 491 514 15709967
- Fishilevich E Domingos AI Asahina K Naef F Vosshall LB Louis M 2005 Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila Curr Biol 15 2086 96 16332533
- Fishilevich E Vosshall LB 2005 Genetic and functional subdivision of the Drosophila antennal lobe Curr Biol 15 1548 53 16139209
- Goldman AL van der Goes van Naters W Lessing D Warr CG Carlson JR 2005 Coexpression of two functional odor receptors in one neuron Neuron 45 661 66 15748842
- Gouwens NW Wilson RI 2009 Signal propagation in Drosophila central neurons J Neurosci 29 6239 49 19439602 PMC2709801
- Gu H Jiang SA Campusano JM Iniguez J Su H 2009 Cav2-type calcium channels encoded by cac regulate AP-independent neurotransmitter release at cholinergic synapses in adult Drosophila brain J Neurophysiol 101 42 53 19004991 PMC2637009
- Ha TS Smith DP 2006 A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila J Neurosci 26 8727 33 16928861 PMC6674374
- Haddad R Weiss T Khan R Nadler B Mandairon N 2010 Global features of neural activity in the olfactory system form a parallel code that predicts olfactory behavior and perception J Neurosci 30 9017 26 20610736 PMC6632474
- Hallem EA Carlson JR 2006 Coding of odors by a receptor repertoire Cell 125 143 60 16615896
- Hallem EA Ho MG Carlson JR 2004 The molecular basis of odor coding in the Drosophila antenna Cell 117 965 79 15210116
- Ignell R Root CM Birse RT Wang JW Nassel DR Winther AM 2009 Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila Proc Natl Acad Sci USA 106 13070 75 19625621 PMC2722350
- Jefferis GS Marin EC Stocker RF Luo L 2001 Target neuron prespecification in the olfactory map of Drosophila Nature 414 204 8 11719930
- Jefferis GS Potter CJ Chan AM Marin EC Rohlfing T 2007 Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation Cell 128 1187 203 17382886 PMC1885945
- Johnson BN Mainland JD Sobel N 2003 Rapid olfactory processing implicates subcortical control of an olfactomotor system J Neurophysiol 90 1084 94 12711718
- Kazama H Wilson RI 2008 Homeostatic matching and nonlinear amplification at genetically-identified central synapses Neuron 58 401 13 18466750 PMC2429849
- Kazama H Wilson RI 2009 Origins of correlated activity in an olfactory circuit Nat Neurosci 12 1136 44 19684589 PMC2751859
- Kazama H Yaksi E Wilson RI 2011 Cell death triggers olfactory circuit plasticity via glial signaling in Drosophila J Neurosci 31 7619 30 21613475 PMC3119471
- Kim AJ Lazar AA Slutskiy YB 2011 System identification of Drosophila olfactory sensory neurons J Comput Neurosci 30 143 61 20730480 PMC3736744
- Kim DH Phillips ME Chang AY Patel HK Nguyen KT Willhite DC 2011 Lateral connectivity in the olfactory bulb is sparse and segregated Front Neural Circuits 5 5 21559072 PMC3084525
- Kreher SA Mathew D Kim J Carlson JR 2008 Translation of sensory input into behavioral output via an olfactory system Neuron 59 110 24 18614033 PMC2496968
- Lai SL Awasaki T Ito K Lee T 2008 Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage Development 135 2883 93 18653555
- Larsson MC Domingos AI Jones WD Chiappe ME Amrein H Vosshall LB 2004 Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction Neuron 43 703 14 15339651
- Laughlin S 1981 A simple coding procedure enhances a neuron’s information capacity Z Naturforsch C 36 910 12 7303823
- Laurent G 2002 Olfactory network dynamics and the coding of multidimensional signals Nat Rev Neurosci 3 884 95 12415296
- Liu M Chen TY Ahamed B Li J Yau KW 1994 Calcium-calmodulin modulation of the olfactory cyclic nucleotide-gated cation channel Science 266 1348 54 7526466
- Luo SX Axel R Abbott LF 2010 Generating sparse and selective third-order responses in the olfactory system of the fly Proc Natl Acad Sci USA 107 10713 18 20498080 PMC2890779
- Martin JP Beyerlein A Dacks AM Reisenman CE Riffell JA 2011 The neurobiology of insect olfaction: sensory processing in a comparative context Prog Neurobiol 95 427 47 21963552
- Masek P Heisenberg M 2008 Distinct memories of odor intensity and quality in Drosophila Proc Natl Acad Sci USA 105 15985 90 18824685 PMC2556361
- Miesenböck G 2004 Genetic methods for illuminating the function of neural circuits Curr Opin Neurobiol 14 395 402 15194122
- Mu L Ito K Bacon JP Strausfeld NJ 2012 Optic glomeruli and their inputs in Drosophila share an organizational ground pattern with the antennal lobes J Neurosci 32 6061 71 22553013 PMC3358351
- Murphy GJ Glickfeld LL Balsen Z Isaacson JS 2004 Sensory neuron signaling to the brain: properties of transmitter release from olfactory nerve terminals J Neurosci 24 3023 30 15044541 PMC6729835
- Nagel KI Wilson RI 2011 Biophysical mechanisms underlying olfactory receptor neuron dynamics Nat Neurosci 14 208 16 21217763 PMC3030680
- Nassel DR Enell LE Santos JG Wegener C Johard HA 2008 A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions BMC Neurosci 9 90 18803813 PMC2569041
- Ng M Roorda RD Lima SQ Zemelman BV Morcillo P Miesenböck G 2002 Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly Neuron 36 463 74 12408848
- Nitz DA van Swinderen B Tononi G Greenspan RJ 2002 Electrophysiological correlates of rest and activity in Drosophilamelanogaster Curr Biol 12 1934 40 12445387
- Olsen SR Bhandawat V Wilson RI 2007 Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe Neuron 54 89 103 17408580 PMC2048819
- Olsen SR Wilson RI 2008 Lateral presynaptic inhibition mediates gain control in an olfactory circuit Nature 452 956 60 18344978 PMC2824883
- Padmanabhan K Urban NN 2010 Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content Nat Neurosci 13 1276 82 20802489 PMC2975253
- Parker AJ Newsome WT 1998 Sense and the single neuron: probing the physiology of perception Annu Rev Neurosci 21 227 77 9530497
- Reisert J 2010 Origin of basal activity in mammalian olfactory receptor neurons J Gen Physiol 136 529 40 20974772 PMC2964517
- Reisert J Matthews HR 2000 Adaptation-induced changes in sensitivity in frog olfactory receptor cells Chem Senses 25 483 86 10944514
- Reisert J Restrepo D 2009 Molecular tuning of odorant receptors and its implication for odor signal processing Chem Senses 34 535 45 19525317 PMC2733323
- Rohrbough J Broadie K 2002 Electrophysiological analysis of synaptic transmission in central neurons of Drosophila larvae J Neurophysiol 88 847 60 12163536
- Root CM Ko KI Jafari A Wang JW 2011 Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search Cell 145 133 44 21458672 PMC3073827
- Root CM Masuyama K Green DS Enell LE Nassel DR 2008 A presynaptic gain control mechanism fine-tunes olfactory behavior Neuron 59 311 21 18667158 PMC2539065
- Root CM Semmelhack JL Wong AM Flores J Wang JW 2007 Propagation of olfactory information in Drosophila Proc Natl Acad Sci USA 104 11826 31 17596338 PMC1913902
- Sachse S Rueckert E Keller A Okada R Tanaka NK 2007 Activity-dependent plasticity in an olfactory circuit Neuron 56 838 50 18054860
- Saito H Chi Q Zhuang H Matsunami H Mainland JD 2009 Odor coding by a mammalian receptor repertoire Sci Signal 2 ra9 19261596 PMC2774247
- Sato K Pellegrino M Nakagawa T Nakagawa T Vosshall LB Touhara K 2008 Insect olfactory receptors are heteromeric ligand-gated ion channels Nature 452 1002 6 18408712
- Schlief ML Wilson RI 2007 Olfactory processing and behavior downstream from highly selective receptor neurons Nat Neurosci 10 623 30 17417635 PMC2838507
- Schoenfeld TA Cleland TA 2005 The anatomical logic of smell Trends Neurosci 28 620 27 16182387
- Schuckel J French AS 2008 A digital sequence method of dynamic olfactory characterization J Neurosci Methods 171 98 103 18395266
- Schuckel J Meisner S Torkkeli PH French AS 2008 Dynamic properties of Drosophila olfactory electroantennograms J Comp Physiol A 194 483 89 18320197
- Schuckel J Torkkeli PH French AS 2009 Two interacting olfactory transduction mechanisms have linked polarities and dynamics in Drosophilamelanogaster antennal basiconic sensilla neurons J Neurophysiol 102 214 23 19403747
- Scott JW Acevedo HP Sherrill L 2006 Effects of concentration and sniff flow rate on the rat electroolfactogram Chem Senses 31 581 93 16740644 PMC2225541
- Seki Y Rybak J Wicher D Sachse S Hansson BS 2010 Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe J Neurophysiol 104 1007 19 20505124
- Semmelhack JL Wang JW 2009 Select Drosophila glomeruli mediate innate olfactory attraction and aversion Nature 459 218 23 19396157 PMC2702439
- Silbering AF Benton R 2010 Ionotropic and metabotropic mechanisms in chemoreception: ‘chance or design’? EMBO Rep 11 173 79 20111052 PMC2838705
- Silbering AF Galizia CG 2007 Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions J Neurosci 27 11966 77 17978037 PMC6673347
- Silbering AF Okada R Ito K Galizia CG 2008 Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28 13075 87 19052198 PMC6671615
- Silbering AF Rytz R Grosjean Y Abuin L Ramdya P 2011 Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems J Neurosci 31 13357 75 21940430 PMC6623294
- Simoncelli EP 2003 Vision and the statistics of the visual environment Curr Opin Neurobiol 13 144 49 12744966
- Singer JH Glowatzki E Moser T Strowbridge BW Bhandawat V Sampath AP 2009 Functional properties of synaptic transmission in primary sense organs J Neurosci 29 12802 6 19828792 PMC2788503
- Smart R Kiely A Beale M Vargas E Carraher C 2008 Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins Insect Biochem Mol Biol 38 770 80 18625400
- Smear M Shusterman R O’Connor R Bozza T Rinberg D 2011 Perception of sniff phase in mouse olfaction Nature 479 397 400 21993623
- Sobel EC Tank DW 1993 Timing of odor stimulation does not alter patterning of olfactory bulb unit activity in freely breathing rats J Neurophysiol 69 1331 37 8492167
- Soucy ER Albeanu DF Fantana AL Murthy VN Meister M 2009 Precision and diversity in an odor map on the olfactory bulb Nat Neurosci 12 210 20 19151709
- Stocker RF 1994 The organization of the chemosensory system in Drosophilamelanogaster: a review Cell Tissue Res 275 3 26 8118845
- Stocker RF 2008 Design of the larval chemosensory system Adv Exp Med Biol 628 69 81 18683639
- Stocker RF Lienhard MC Borst A Fischbach KF 1990 Neuronal architecture of the antennal lobe in Drosophilamelanogaster Cell Tissue Res 262 9 34 2124174
- Stortkuhl KF Hovemann BT Carlson JR 1999 Olfactory adaptation depends on the Trp Ca2+ channel in Drosophila J Neurosci 19 4839 46 10366618 PMC6782652
- Stuart GJ Dodt HU Sakmann B 1993 Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy Pflugers Arch 423 511 18 8351200
- Su CY Menuz K Carlson JR 2009 Olfactory perception: receptors, cells, and circuits Cell 139 45 59 19804753 PMC2765334
- Suh GS Ben-Tabou de Leon S Tanimoto H Fiala A Benzer S Anderson DJ 2007 Light activation of an innate olfactory avoidance response in Drosophila Curr Biol 17 905 8 17493811
- Tan J Savigner A Ma M Luo M 2010 Odor information processing by the olfactory bulb analyzed in gene-targeted mice Neuron 65 912 26 20346765 PMC2901914
- Tanaka NK Awasaki T Shimada T Ito K 2004 Integration of chemosensory pathways in the Drosophila second-order olfactory centers Curr Biol 14 449 57 15043809
- Tanaka NK Ito K Stopfer M 2009 Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons J Neurosci 29 8595 603 19571150 PMC2753235
- Turner GC Bazhenov M Laurent G 2007 Olfactory representations by Drosophila mushroom body neurons J Neurophysiol 99 734 46 18094099
- Turner SL Ray A 2009 Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants Nature 461 277 81 19710651
- Uchida N Mainen ZF 2003 Speed and accuracy of olfactory discrimination in the rat Nat Neurosci 6 1224 29 14566341
- van der Goes van Naters W Carlson JR 2007 Receptors and neurons for fly odors in Drosophila Curr Biol 17 606 12 17363256 PMC1876700
- Vosshall LB Amrein H Morozov PS Rzhetsky A Axel R 1999 A spatial map of olfactory receptor expression in the Drosophila antenna Cell 96 725 36 10089887
- Vosshall LB Wong AM Axel R 2000 An olfactory sensory map in the fly brain Cell 102 147 59 10943836
- Wang JW Wong AM Flores J Vosshall LB Axel R 2003 Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain Cell 112 271 82 12553914
- Wang Y Wright NJ Guo H Xie Z Svoboda K 2001 Genetic manipulation of the odor-evoked distributed neural activity in the Drosophila mushroom body Neuron 29 267 76 11182097
- Wark B Lundstrom BN Fairhall A 2007 Sensory adaptation Curr Opin Neurobiol 17 423 29 17714934 PMC2084204
- Wicher D Schafer R Bauernfeind R Stensmyr MC Heller R 2008 Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels Nature 452 1007 11 18408711
- Wilson RI Laurent G 2005 Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe J Neurosci 25 9069 79 16207866 PMC6725763
- Wilson RI Turner GC Laurent G 2004 Transformation of olfactory representations in the Drosophila antennal lobe Science 303 366 70 14684826
- Winther AM Acebes A Ferrus A 2006 Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila Mol Cell Neurosci 31 399 406 16289899
- Winther AM Siviter RJ Isaac RE Predel R Nassel DR 2003 Neuronal expression of tachykinin-related peptides and gene transcript during postembryonic development of Drosophila J Comp Neurol 464 180 96 12898611
- Xu P Atkinson R Jones DN Smith DP 2005 Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons Neuron 45 193 200 15664171
- Yaksi E Wilson RI 2010 Electrical coupling between olfactory glomeruli Neuron 67 1034 47 20869599 PMC2954501
- Yao CA Carlson JR 2010 Role of G-proteins in odor-sensing and CO2-sensing neurons in Drosophila J Neurosci 30 4562 72 20357107 PMC2858456
- Yao CA Ignell R Carlson JR 2005 Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna J Neurosci 25 8359 67 16162917 PMC6725686
- Yarali A Ehser S Hapil FZ Huang J Gerber B 2009 Odour intensity learning in fruit flies Proc Biol Sci 276 3413 20 19586944 PMC2817181
- Yasuyama K Salvaterra PM 1999 Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system Microsc Res Tech 45 65 79 10332725
- Yu D Ponomarev A Davis RL 2004 Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment Neuron 42 437 49 15134640
- Zhou Y Wilson RI 2012 Transduction in Drosophila olfactory receptor neurons is invariant to air speed J Neurophysiol 108 2051 59 22815404 PMC3544999
Cited by
Sorted by citations
Ring attractor dynamics in the <i>Drosophila</i> central brain
Kim, S. S., Rouault, H., Druckmann, S., & Jayaraman, V. (2017) · Science · doi:10.1126/science.aal4835 · Cited by 417 · see citing works
A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
Seeds, A. M., Ravbar, P., Chung, P., Hampel, S., Midgley, F. M., Mensh, B. D., & Simpson, J. H. (2014) · eLife · doi:10.7554/elife.02951 · Cited by 200 · see citing works
Gustatory Processing in <i>Drosophila melanogaster</i>
Scott, K. (2018) · Annual Review of Entomology · doi:10.1146/annurev-ento-020117-043331 · Cited by 215 · 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
Chemoreceptor co-expression in Drosophila melanogaster olfactory neurons
Task, D., Lin, C.-C., Vulpe, A., Afify, A., Ballou, S., Brbic, M., Schlegel, P., Raji, J., Jefferis, G. S., Li, H., et al. (2022) · eLife · doi:10.7554/elife.72599 · Cited by 141 · see citing works
The function and organization of the motor system controlling flight maneuvers in flies
Lindsay, T., Sustar, A., & Dickinson, M. (2017) · Current Biology · doi:10.1016/j.cub.2016.12.018 · Cited by 103 · see citing works
Olfactory Sensing and Navigation in Turbulent Environments
Reddy, G., Murthy, V. N., & Vergassola, M. (2022) · Annual Review of Condensed Matter Physics · doi:10.1146/annurev-conmatphys-031720-032754 · Cited by 100 · see citing works
Simultaneous Encoding of Odors by Channels with Diverse Sensitivity to Inhibition
Hong, E. J., & Wilson, R. I. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.040 · Cited by 93 · see citing works
Self-citationA resource for the Drosophila antennal lobe provided by the connectome of glomerulus VA1v
Horne, J. A., Langille, C., McLin, S., Wiederman, M., Lu, Z., Xu, C. S., Plaza, S. M., Scheffer, L. K., Hess, H. F., & Meinertzhagen, I. A. (2018) · eLife · doi:10.7554/elife.37550 · Cited by 46 · see citing works
Evolving the olfactory system with machine learning
Wang, P. Y., Sun, Y., Axel, R., Abbott, L. F., & Yang, G. R. (2021) · Neuron · doi:10.1016/j.neuron.2021.09.010 · Cited by 54 · see citing works
Huoviala, P., Dolan, M.-J., Love, F. M., Myers, P., Frechter, S., Namiki, S., Pettersson, L., Roberts, R. J. V., Turnbull, R., Mitrevica, Z., et al. (2018) · doi:10.1101/394403 · Cited by 43 · see citing works
NeuroMechFly v2: simulating embodied sensorimotor control in adult Drosophila
Wang-Chen, S., Stimpfling, V. A., Lam, T. K. C., Özdil, P. G., Genoud, L., Hurtak, F., & Ramdya, P. (2024) · Nature Methods · doi:10.1038/s41592-024-02497-y · Cited by 43 · see citing works
“ORNs detect specific odorant molecules and convey this information to the brain’s antennal lobe, where it is further processed 44 .”
Olfactory stimuli and moonwalker SEZ neurons can drive backward locomotion in Drosophila
Israel, S., Rozenfeld, E., Weber, D., Huetteroth, W., & Parnas, M. (2022) · Current Biology · doi:10.1016/j.cub.2022.01.035 · Cited by 26 · see citing works
- Authors
- Wilson, R. I.
- Affiliations
- Harvard University (US)
- Corresponding author
- Wilson, Rachel I.
- ORCID
- Wilson, Rachel I.
- Venue
- Annual Review of Neuroscience
- Publisher
- Annual Reviews
- Published
- 2013-07-08
- Volume
- 36
- Issue
- 1
- Pages
- 217-241
- ISSN
- 0147-006X (ISSN-L)
- 1545-4126
- PMC
- PMC3933953
- OpenAlex
- W2158976454
- Cited by
- 394
- References
- 10
- Citations by year
- 2026: 19 · 2025: 32 · 2024: 28 · 2023: 43 · 2022: 27 · 2021: 47 · 2020: 39 · 2019: 24 · 2018: 28 · 2017: 34 · 2016: 26 · 2015: 24 · 2014: 19 · 2013: 4
- FWCI
- 2.47
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Annual Review of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute on Deafness and Other Communication Disorders (R01DC008174)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Drosophila olfaction, olfactory sensory neurons, antennal lobe, odor coding, synaptic mechanisms, neural adaptation, environmental statistics, early sensory processing
- MeSH terms
- Animals, Drosophila, Odorants, Olfactory Pathways, Smell, Olfactory Receptor 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