No retraction, correction or concern found when last checked on Nov 4, 2026.
The wiring diagram of a glomerular olfactory system
Matthew E Berck, Avinash Khandelwal, Lindsey Claus and 9 more
eLife · 2016 · CC BY
Abstract
The sense of smell enables animals to react to long-distance cues according to learned and innate valences. Here, we have mapped with electron microscopy the complete wiring diagram of the Drosophila larval antennal lobe, an olfactory neuropil similar to the vertebrate olfactory bulb. We found a canonical circuit with uniglomerular projection neurons (uPNs) relaying gain-controlled ORN activity to the mushroom body and the lateral horn. A second, parallel circuit with multiglomerular projection neurons (mPNs) and hierarchically connected local neurons (LNs) selectively integrates multiple ORN signals already at the first synapse. LN-LN synaptic connections putatively implement a bistable gain control mechanism that either computes odor saliency through panglomerular inhibition, or allows some glomeruli to respond to faint aversive odors in the presence of strong appetitive odors. This complete wiring diagram will support experimental and theoretical studies towards bridging the gap between circuits and behavior.
References 79
- 1.
Alon U. Network motifs: theory and experimental approaches. Nature Reviews. Genetics. 2007;8:450-461.
Not in our library10.1038/nrg2102
- 2.
- 3.
Balu R, Pressler RT, Strowbridge BW. Multiple modes of synaptic excitation of olfactory bulb granule cells. Journal of Neuroscience. 2007;27:5621-5632.
Not in our library10.1523/jneurosci.4630-06.2007
- 4.
- 5.
Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nature Neuroscience. 2007;10:1474-1482.
Not in our library10.1038/nn1976
- 6.
Carandini M. From circuits to behavior: a bridge too far? Nature Neuroscience. 2012;15:507-509.
Not in our library10.1038/nn.3043
- 7.
Chou YH, Spletter ML, Yaksi E, Leong JC, Wilson RI, Luo L. Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nature Neuroscience. 2010;13:439-449.
Not in our library10.1038/nn.2489
- 8.
Cobb M. What and how do maggots smell? Biological Reviews. 1999;74:425-459.
Not in our library10.1017/s0006323199005393
- 9.
Dacks AM, Green DS, Root CM, Nighorn AJ, Wang JW. Serotonin modulates olfactory processing in the antennal lobe of Drosophila. Journal of Neurogenetics. 2009;23:366-377.
Not in our library10.3109/01677060903085722
- 10.
Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, DiAntonio A. Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. Journal of Neuroscience. 2004;24:10466-10474.
Not in our library10.1523/jneurosci.3001-04.2004
- 11.
Das A, Gupta T, Davla S, Prieto-Godino LL, Diegelmann S, Reddy OV, Raghavan KV, Reichert H, Lovick J, Hartenstein V. Neuroblast lineage-specific origin of the neurons of the Drosophila larval olfactory system. Developmental Biology. 2013;373:322-337.
Not in our library10.1016/j.ydbio.2012.11.003
- 12.
de Belle JS, Heisenberg M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science. 1994;263:692-695.
Not in our library10.1126/science.8303280
- 13.
Distler PG, Boeckh J. Synaptic connection between olfactory receptor cells and uniglomerular projection neurons in the antennal lobe of the American cockroach, Periplaneta americana. The Journal of Comparative Neurology. 1996;370:35-46.
Not in our library10.1002/(sici)1096-9861(19960617)370:1<35::aid-cne4>3.0.co;2-m
- 14.
Drobysheva D, Ameel K, Welch B, Ellison E, Chaichana K, Hoang B, Sharma S, Neckameyer W, Srinakevitch I, Murphy KJ, Schmid A. An optimized method for histological detection of dopaminergic neurons in Drosophila melanogaster. Journal of Histochemistry and Cytochemistry. 2008;56:1049-1063.
Not in our library10.1369/jhc.2008.951137
- 15.
- 16.
Fischbach K, Heisenberg M. Neurogenetics and behaviour in insects. Journal of Experimental Biology. 1984;112:65-93.
Not in our library
- 17.
Fishilevich E, Domingos AI, Asahina K, Naef F, Vosshall LB, Louis M. Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Current Biology. 2005;15:2086-2096.
Not in our library10.1016/j.cub.2005.11.016
- 18.
Fişek M, Wilson RI. Stereotyped connectivity and computations in higher-order olfactory neurons. Nature Neuroscience. 2014;17:280-288.
Not in our library10.1038/nn.3613
- 19.
Friedrich RW, Korsching SI. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron. 1997;18:737-752.
Not in our library10.1016/s0896-6273(00)80314-1
- 20.
Gao XJ, Clandinin TR, Luo L. Extremely sparse olfactory inputs are sufficient to mediate innate aversion in Drosophila. PloS One. 2015;10:e14859.
Not in our library10.1371/journal.pone.0125986
- 21.
Gepner R, Mihovilovic Skanata M, Bernat NM, Kaplow M, Gershow M, Skanata MM. Computations underlying Drosophila photo-taxis, odor-taxis, and multi-sensory integration. eLife. 2015;4:e14859.
Not in our library10.7554/elife.06229
- 22.
Gerber B, Stocker RF. The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chemical Senses. 2007;32:65-89.
Not in our library10.1093/chemse/bjl030
- 23.
Gershow M, Berck M, Mathew D, Luo L, Kane EA, Carlson JR, Samuel AD. Controlling airborne cues to study small animal navigation. Nature Methods. 2012;9:290-296.
Not in our library10.1038/nmeth.1853
- 24.
Gomez-Marin A, Stephens GJ, Louis M. Active sampling and decision making in Drosophila chemotaxis. Nature Communications. 2011;2:441.
Not in our library10.1038/ncomms1455
- 25.
Gouwens NW, Wilson RI. Signal propagation in Drosophila central neurons. Journal of Neuroscience. 2009;29:6239-6249.
Not in our library10.1523/jneurosci.0764-09.2009
- 26.
Haddad R, Khan R, Takahashi YK, Mori K, Harel D, Sobel N. A metric for odorant comparison. Nature Methods. 2008;5:425-429.
Not in our library10.1038/nmeth.1197
- 27.
Haddad R, Weiss T, Khan R, Nadler B, Mandairon N, Bensafi M, Schneidman E, Sobel N. Global features of neural activity in the olfactory system form a parallel code that predicts olfactory behavior and perception. Journal of Neuroscience. 2010;30:9017-9026.
Not in our library10.1523/jneurosci.0398-10.2010
- 28.
Heisenberg M, Borst A, Wagner S, Byers D. Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics. 1985;2:1-30.
Not in our library10.3109/01677068509100140
- 29.
Hernandez-Nunez L, Belina J, Klein M, Si G, Claus L, Carlson JR, Samuel AD. Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics. eLife. 2015;4:e14859.
Not in our library10.7554/elife.06225
- 30.
Kim AJ, Lazar AA, Slutskiy YB. Projection neurons in Drosophila antennal lobes signal the acceleration of odor concentrations. eLife. 2015;4:e14859.
Not in our library10.7554/elife.06651
- 31.
Kreher SA, Mathew D, Kim J, Carlson JR. Translation of sensory input into behavioral output via an olfactory system. Neuron. 2008;59:110-124.
Not in our library10.1016/j.neuron.2008.06.010
- 32.
Lei H, Christensen TA, Hildebrand JG. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nature Neuroscience. 2002;5:557-565.
Not in our library10.1038/nn859
- 33.
Li HH, Kroll JR, Lennox SM, Ogundeyi O, Jeter J, Depasquale G, Truman JW. A GAL4 driver resource for developmental and behavioral studies on the larval CNS of Drosophila. Cell Reports. 2014;8:897-908.
Not in our library10.1016/j.celrep.2014.06.065
- 34.
Liang L, Li Y, Potter CJ, Yizhar O, Deisseroth K, Tsien RW, Luo L. GABAergic projection neurons route selective olfactory inputs to specific higher-order neurons. Neuron. 2013;79:917-931.
Not in our library10.1016/j.neuron.2013.06.014
- 35.
Linster C, Smith BH. A computational model of the response of honey bee antennal lobe circuitry to odor mixtures: overshadowing, blocking and unblocking can arise from lateral inhibition. Behavioural Brain Research. 1997;87:1-14.
Not in our library10.1016/s0166-4328(96)02271-1
- 36.
Liu WW, Wilson RI. Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system. Proceedings of the National Academy of Sciences of the United States of America. 2013;110:10294-10299.
Not in our library10.1073/pnas.1220560110
- 37.
Louis M, Huber T, Benton R, Sakmar TP, Vosshall LB. Bilateral olfactory sensory input enhances chemotaxis behavior. Nature Neuroscience. 2008;11:187-199.
Not in our library10.1038/nn2031
- 38.
Luo SX, Axel R, Abbott LF. Generating sparse and selective third-order responses in the olfactory system of the fly. Proceedings of the National Academy of Sciences of the United States of America. 2010;107:10713-10718.
Not in our library10.1073/pnas.1005635107
- 39.
Manning L, Heckscher ES, Purice MD, Roberts J, Bennett AL, Kroll JR, Pollard JL, Strader ME, Lupton JR, Dyukareva AV, Doan PN, Bauer DM, Wilbur AN, Tanner S, Kelly JJ, Lai SL, Tran KD, Kohwi M, Laverty TR, Pearson JC, Crews ST, Rubin GM, Doe CQ. A resource for manipulating gene expression and analyzing cis-regulatory modules in the Drosophila CNS. Cell Reports. 2012;2:1002-1013.
Not in our library10.1016/j.celrep.2012.09.009
- 40.
Masuda-Nakagawa LM, Gendre N, O'Kane CJ, Stocker RF. Localized olfactory representation in mushroom bodies of Drosophila larvae. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:10314-10319.
Not in our library10.1073/pnas.0900178106
Cited by papers we hold 11
- Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster · 2024No notice
- The connectome of an insect brain · 2023No notice
- Chemoreceptor co-expression in Drosophila melanogaster olfactory neurons · 2022No notice
- Information flow, cell types and stereotypy in a full olfactory connectome · 2021No notice
- Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain · 2020No notice
- The natverse, a versatile toolbox for combining and analysing neuroanatomical data · 2020No notice
- FluoEM, virtual labeling of axons in three-dimensional electron microscopy data for long-range connectomics · 2018Not checked
- Cellular diversity in the Drosophila midbrain revealed by single-cell transcriptomics · 2018No notice
- Functional architecture of reward learning in mushroom body extrinsic neurons of larval Drosophila · 2018No notice
- Wiring variations that enable and constrain neural computation in a sensory microcircuit · 2017No notice
- Synaptic transmission parallels neuromodulation in a central food-intake circuit · 2016No notice
Reads
Read by people on this page
None yet.
Checked or read by AI through naulon
None yet.
A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.
Are you an author?
Is this your paper?
Claim it to add your note and be paid when agents cite it. Free.