Generating parallel representations of position and identity in the olfactory system.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
08 06 2023
Historique:
received: 27 05 2022
revised: 07 12 2022
accepted: 28 04 2023
medline: 12 6 2023
pubmed: 27 5 2023
entrez: 26 5 2023
Statut: ppublish

Résumé

In Drosophila, a dedicated olfactory channel senses a male pheromone, cis-vaccenyl acetate (cVA), promoting female courtship while repelling males. Here, we show that separate cVA-processing streams extract qualitative and positional information. cVA sensory neurons respond to concentration differences in a 5-mm range around a male. Second-order projection neurons encode the angular position of a male by detecting inter-antennal differences in cVA concentration, which are amplified through contralateral inhibition. At the third circuit layer, we identify 47 cell types with diverse input-output connectivity. One population responds tonically to male flies, a second is tuned to olfactory looming, while a third integrates cVA and taste to coincidentally promote female mating. The separation of olfactory features resembles the mammalian what and where visual streams; together with multisensory integration, this enables behavioral responses appropriate to specific ethological contexts.

Identifiants

pubmed: 37236194
pii: S0092-8674(23)00472-5
doi: 10.1016/j.cell.2023.04.038
pmc: PMC10403364
pii:
doi:

Substances chimiques

Drosophila Proteins 0
Receptors, Odorant 0
cis-vaccenyl acetate 0
Pheromones 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2556-2573.e22

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC-U105188491
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203261/Z/16/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 110232/Z/15/Z
Pays : United Kingdom

Informations de copyright

Copyright © 2023 MRC Laboratory of Molecular Biology. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Nat Metab. 2020 Sep;2(9):958-973
pubmed: 32868922
Science. 1970 Feb 27;167(3922):1262
pubmed: 5411913
Curr Biol. 2019 Oct 7;29(19):3200-3215.e5
pubmed: 31564492
J Exp Biol. 2014 Aug 1;217(Pt 15):2796-805
pubmed: 24902744
PeerJ. 2018 Sep 27;6:e5585
pubmed: 30280017
Curr Biol. 2018 Aug 20;28(16):2624-2631.e5
pubmed: 30078566
Bioinformatics. 2011 Sep 1;27(17):2453-4
pubmed: 21727141
Neuron. 2019 May 22;102(4):828-842.e7
pubmed: 30948249
Front Physiol. 2019 Jul 09;10:851
pubmed: 31354516
Curr Biol. 2010 Sep 28;20(18):1602-14
pubmed: 20832315
Cell. 2013 Dec 19;155(7):1610-23
pubmed: 24360281
Neuron. 2016 Jul 20;91(2):293-311
pubmed: 27373836
Cell Rep. 2012 Oct 25;2(4):991-1001
pubmed: 23063364
Nature. 2010 Dec 2;468(7324):686-90
pubmed: 21124455
Elife. 2017 May 22;6:
pubmed: 28530904
Nat Methods. 2020 Dec;17(12):1254-1261
pubmed: 33139893
Elife. 2022 May 25;11:
pubmed: 35611959
Nature. 2010 Jan 14;463(7278):227-31
pubmed: 19966787
Elife. 2020 Nov 23;9:
pubmed: 33225998
Elife. 2020 Sep 07;9:
pubmed: 32880371
Curr Opin Neurobiol. 2018 Dec;53:120-130
pubmed: 30059820
Neuron. 2017 Aug 30;95(5):1112-1128.e7
pubmed: 28858617
Curr Biol. 2010 Sep 28;20(18):1589-601
pubmed: 20832311
J Appl Physiol. 1964 May;19:369-73
pubmed: 14173530
Neuron. 2011 Feb 10;69(3):498-508
pubmed: 21315260
Nature. 2004 Aug 12;430(7001):781-5
pubmed: 15306810
Biomed Eng Online. 2003 May 17;2:13
pubmed: 12801419
Elife. 2020 Apr 14;9:
pubmed: 32286229
Nat Methods. 2014 Mar;11(3):338-46
pubmed: 24509633
Neuron. 2015 Sep 2;87(5):1036-49
pubmed: 26279475
Nat Rev Neurosci. 2016 Oct 18;17(11):692-704
pubmed: 27752072
Nature. 2007 Mar 29;446(7135):542-6
pubmed: 17392786
Neuron. 1999 Sep;24(1):95-104, 111-25
pubmed: 10677030
Elife. 2021 May 25;10:
pubmed: 34032214
Nature. 2008 Mar 27;452(7186):473-7
pubmed: 18305480
Elife. 2018 Oct 11;7:
pubmed: 30307393
Curr Biol. 2019 Mar 18;29(6):1073-1081.e4
pubmed: 30827912
Neuron. 2012 Jul 26;75(2):320-9
pubmed: 22841316
Nature. 2017 Nov 8;551(7679):237-241
pubmed: 29120418
Trends Neurosci. 1992 Jan;15(1):20-5
pubmed: 1374953
Cell. 2018 Jul 26;174(3):730-743.e22
pubmed: 30033368
Front Neuroinform. 2015 Apr 08;9:7
pubmed: 25904861
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Neurosci Methods. 2014 Mar 30;225:106-19
pubmed: 24491637
Nat Commun. 2020 Oct 22;11(1):5350
pubmed: 33093442
Neuron. 2014 Aug 20;83(4):850-65
pubmed: 25123314
Curr Biol. 2019 May 6;29(9):1545-1550.e2
pubmed: 31031119
Elife. 2015 Dec 29;4:
pubmed: 26714106
Comput Biomed Res. 1996 Jun;29(3):162-73
pubmed: 8812068
Nature. 2021 Jan;589(7843):577-581
pubmed: 33239786
Cell. 2007 Mar 23;128(6):1187-203
pubmed: 17382886
Nature. 2020 Mar;579(7797):101-105
pubmed: 32103180
Cell Tissue Res. 1983;232(2):237-48
pubmed: 6411344
J Neurosci. 2001 Dec 1;21(23):9455-9
pubmed: 11717379
PLoS One. 2015 Aug 07;10(8):e0135186
pubmed: 26252206
Nat Neurosci. 2018 Sep;21(9):1281-1289
pubmed: 30127430
Nature. 2013 Jan 17;493(7432):424-8
pubmed: 23263180
Neuron. 2004 Sep 2;43(5):703-14
pubmed: 15339651
Sci Rep. 2016 Feb 25;6:21841
pubmed: 26912260
Proc Natl Acad Sci U S A. 2019 Mar 19;116(12):5715-5720
pubmed: 30837311
Cell. 2002 Apr 19;109(2):243-55
pubmed: 12007410
Nat Commun. 2018 Oct 12;9(1):4252
pubmed: 30315166
J Neurosci Methods. 2017 Nov 1;291:83-94
pubmed: 28782629
PLoS One. 2020 Dec 31;15(12):e0236495
pubmed: 33382698
Cell. 2014 Jan 16;156(1-2):221-35
pubmed: 24439378
Elife. 2019 May 21;8:
pubmed: 31112130
Curr Opin Neurobiol. 2016 Jun;38:18-26
pubmed: 26851712
Elife. 2020 Nov 03;9:
pubmed: 33141021
Nat Neurosci. 2007 Nov;10(11):1474-82
pubmed: 17922008
Cell. 2017 Jul 13;170(2):393-406.e28
pubmed: 28709004
Neurosci Bull. 2023 Mar 21;:
pubmed: 36941515
Nature. 2022 Jan;601(7894):595-599
pubmed: 34937941
Neuron. 2020 Jan 22;105(2):322-333.e5
pubmed: 31810837
Curr Biol. 2014 Feb 3;24(3):242-51
pubmed: 24440391
Commun Biol. 2020 Apr 1;3(1):150
pubmed: 32238904
Neuron. 2014 Jul 2;83(1):149-63
pubmed: 24991959
PLoS Biol. 2019 Jan 10;17(1):e2006012
pubmed: 30629594
Proc Natl Acad Sci U S A. 2015 May 26;112(21):E2829-35
pubmed: 25964351
J Neurosci. 2018 Oct 31;38(44):9383-9389
pubmed: 30381430
Methods Mol Biol. 2016;1478:53-78
pubmed: 27730575
Curr Biol. 2020 Aug 17;30(16):3183-3199.e6
pubmed: 32619485
Bioinformatics. 2009 Aug 1;25(15):1984-6
pubmed: 19376822
Nat Methods. 2013 Jan;10(1):64-7
pubmed: 23202433
Curr Biol. 2013 Jul 8;23(13):1202-8
pubmed: 23770187
Nat Methods. 2022 Jan;19(1):119-128
pubmed: 34949809
J Chem Ecol. 2016 Aug;42(8):739-747
pubmed: 27539589
J Neurophysiol. 2011 Apr;105(4):1711-21
pubmed: 21289134
Cell. 2002 Apr 19;109(2):229-41
pubmed: 12007409
Nature. 2009 Oct 15;461(7266):987-91
pubmed: 19829381

Auteurs

István Taisz (I)

Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK.

Erika Donà (E)

Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK.

Daniel Münch (D)

Champalimaud Foundation, Lisbon, Portugal.

Shanice N Bailey (SN)

Department of Zoology, University of Cambridge, Cambridge, UK.

Billy J Morris (BJ)

Department of Zoology, University of Cambridge, Cambridge, UK.

Kimberly I Meechan (KI)

Department of Zoology, University of Cambridge, Cambridge, UK.

Katie M Stevens (KM)

Department of Zoology, University of Cambridge, Cambridge, UK.

Irene Varela-Martínez (I)

Department of Zoology, University of Cambridge, Cambridge, UK.

Marina Gkantia (M)

Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK.

Philipp Schlegel (P)

Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK; Department of Zoology, University of Cambridge, Cambridge, UK.

Carlos Ribeiro (C)

Champalimaud Foundation, Lisbon, Portugal.

Gregory S X E Jefferis (GSXE)

Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK; Department of Zoology, University of Cambridge, Cambridge, UK. Electronic address: jefferis@mrc-lmb.cam.ac.uk.

Dana S Galili (DS)

Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK. Electronic address: dgalili@mrc-lmb.cam.ac.uk.

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