Mushroom body input connections form independently of sensory activity in Drosophila melanogaster.


Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
26 09 2022
Historique:
received: 05 11 2021
revised: 04 05 2022
accepted: 21 07 2022
pubmed: 18 8 2022
medline: 30 9 2022
entrez: 17 8 2022
Statut: ppublish

Résumé

Associative brain centers, such as the insect mushroom body, need to represent sensory information in an efficient manner. In Drosophila melanogaster, the Kenyon cells of the mushroom body integrate inputs from a random set of olfactory projection neurons, but some projection neurons-namely those activated by a few ethologically meaningful odors-connect to Kenyon cells more frequently than others. This biased and random connectivity pattern is conceivably advantageous, as it enables the mushroom body to represent a large number of odors as unique activity patterns while prioritizing the representation of a few specific odors. How this connectivity pattern is established remains largely unknown. Here, we test whether the mechanisms patterning the connections between Kenyon cells and projection neurons depend on sensory activity or whether they are hardwired. We mapped a large number of mushroom body input connections in partially anosmic flies-flies lacking the obligate odorant co-receptor Orco-and in wild-type flies. Statistical analyses of these datasets reveal that the random and biased connectivity pattern observed between Kenyon cells and projection neurons forms normally in the absence of most olfactory sensory activity. This finding supports the idea that even comparatively subtle, population-level patterns of neuronal connectivity can be encoded by fixed genetic programs and are likely to be the result of evolved prioritization of ecologically and ethologically salient stimuli.

Identifiants

pubmed: 35977547
pii: S0960-9822(22)01204-0
doi: 10.1016/j.cub.2022.07.055
pmc: PMC9533768
mid: NIHMS1830680
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

4000-4012.e5

Subventions

Organisme : NIBIB NIH HHS
ID : R01 EB029858
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS106018
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS107970
Pays : United States

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Curr Biol. 2020 Aug 17;30(16):3223-3230.e4
pubmed: 32559450
J Comp Neurol. 2015 Feb 15;523(3):530-44
pubmed: 25327641
Cell. 2012 Dec 7;151(6):1345-57
pubmed: 23217715
Elife. 2014 Dec 23;3:e04577
pubmed: 25535793
Nature. 2007 Mar 29;446(7135):542-6
pubmed: 17392786
Neuron. 2004 Sep 2;43(5):703-14
pubmed: 15339651
Bioinformatics. 2011 Sep 1;27(17):2453-4
pubmed: 21727141
Cell. 2017 May 18;169(5):956-969.e17
pubmed: 28502772
J Neurosci. 2011 May 25;31(21):7619-30
pubmed: 21613475
Curr Biol. 2020 Aug 17;30(16):3183-3199.e6
pubmed: 32619485
Nat Neurosci. 2013 Dec;16(12):1821-9
pubmed: 24141312
Development. 2009 Apr;136(8):1273-82
pubmed: 19304886
MicroPubl Biol. 2021 May 14;2021:
pubmed: 34007957
Elife. 2020 Dec 14;9:
pubmed: 33315010
Curr Biol. 2010 Nov 9;20(21):1938-44
pubmed: 20951043
Elife. 2019 Jun 17;8:
pubmed: 31205005
Elife. 2020 Sep 07;9:
pubmed: 32880371
Elife. 2021 May 25;10:
pubmed: 34032214
Opt Lett. 2008 Jan 15;33(2):156-8
pubmed: 18197224
Curr Biol. 2005 Sep 6;15(17):1535-47
pubmed: 16139208
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Curr Biol. 2005 Sep 6;15(17):1548-53
pubmed: 16139209
PLoS Biol. 2015 Dec 16;13(12):e1002318
pubmed: 26674493
Elife. 2020 Jan 08;9:
pubmed: 31913123
Neuron. 2007 Dec 6;56(5):838-50
pubmed: 18054860
Neuron. 2008 Sep 25;59(6):1009-23
pubmed: 18817738
J Neurosci. 2006 Mar 29;26(13):3367-76
pubmed: 16571743
Cell Rep. 2015 Mar 31;10(12):2083-95
pubmed: 25818295
Cell Rep. 2021 Mar 16;34(11):108871
pubmed: 33730583
Curr Biol. 2021 Dec 20;31(24):5533-5546.e7
pubmed: 34731675
Nat Neurosci. 2005 Jan;8(1):15-7
pubmed: 15592462
IEEE Pac Vis Symp. 2012;:201-208
pubmed: 23584131
J Neurosci. 2011 Sep 21;31(38):13357-75
pubmed: 21940430
Cell. 2017 Aug 10;170(4):727-735.e10
pubmed: 28802042
Curr Biol. 2022 Aug 8;32(15):3334-3349.e6
pubmed: 35797998
Curr Biol. 2017 Aug 7;27(15):2318-2330.e3
pubmed: 28756946
PLoS Biol. 2006 Feb;4(2):e20
pubmed: 16402857
Neuron. 2007 Apr 5;54(1):89-103
pubmed: 17408580
Nature. 2007 Jan 4;445(7123):86-90
pubmed: 17167414
STAR Protoc. 2021 Mar 06;2(1):100381
pubmed: 33733243
Nature. 2013 May 2;497(7447):113-7
pubmed: 23615618
J Neurosci. 2014 Mar 12;34(11):3959-68
pubmed: 24623773
Neuron. 2017 Mar 8;93(5):1153-1164.e7
pubmed: 28215558
Nature. 2014 Aug 7;512(7512):91-5
pubmed: 24896182
J Neurobiol. 2003 Jul;56(1):13-23
pubmed: 12767029
Neural Dev. 2018 Jul 1;13(1):14
pubmed: 29960596
BMC Bioinformatics. 2017 May 26;18(1):280
pubmed: 28549411
J Neurosci. 2001 Aug 15;21(16):6274-82
pubmed: 11487650
Bioessays. 2015 Sep;37(9):996-1004
pubmed: 26184069

Auteurs

Tatsuya Tatz Hayashi (TT)

School of Biological Sciences, University of Utah, Aline Skaggs Wilmot Biology Building, 257 South 1400 East, Salt Lake City, UT 84112, USA; Neuroscience Program, University of Utah, Salt Lake City, UT 84112, USA.

Alexander John MacKenzie (AJ)

School of Biological Sciences, University of Utah, Aline Skaggs Wilmot Biology Building, 257 South 1400 East, Salt Lake City, UT 84112, USA; Neuroscience Program, University of Utah, Salt Lake City, UT 84112, USA.

Ishani Ganguly (I)

Center for Theoretical Neuroscience, Columbia University, Jerome L Greene Science Center, 3227 Broadway, New York, NY 10027, USA.

Kaitlyn Elizabeth Ellis (KE)

School of Biological Sciences, University of Utah, Aline Skaggs Wilmot Biology Building, 257 South 1400 East, Salt Lake City, UT 84112, USA.

Hayley Marie Smihula (HM)

School of Biological Sciences, University of Utah, Aline Skaggs Wilmot Biology Building, 257 South 1400 East, Salt Lake City, UT 84112, USA.

Miles Solomon Jacob (MS)

School of Biological Sciences, University of Utah, Aline Skaggs Wilmot Biology Building, 257 South 1400 East, Salt Lake City, UT 84112, USA.

Ashok Litwin-Kumar (A)

Center for Theoretical Neuroscience, Columbia University, Jerome L Greene Science Center, 3227 Broadway, New York, NY 10027, USA.

Sophie Jeanne Cécile Caron (SJC)

School of Biological Sciences, University of Utah, Aline Skaggs Wilmot Biology Building, 257 South 1400 East, Salt Lake City, UT 84112, USA; Neuroscience Program, University of Utah, Salt Lake City, UT 84112, USA. Electronic address: sophie.caron@utah.edu.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH