OpenLB
Open Library of Bioscience
Advanced Search
eLife
Aug 08, 2017;6

Organization of the larval visual circuit.

Ivan Larderet, Pauline Mj Fritsch, Nanae Gendre, G Larisa Neagu-Maier, Richard D Fetter, Casey M Schneider-Mizell, James W Truman, Marta Zlatic, Albert Cardona, Simon G Sprecher
Author Information
  1. Ivan Larderet: Department of Biology, University of Fribourg, Fribourg, Switzerland.
  2. Pauline Mj Fritsch: Department of Biology, University of Fribourg, Fribourg, Switzerland.
  3. Nanae Gendre: Department of Biology, University of Fribourg, Fribourg, Switzerland.
  4. G Larisa Neagu-Maier: Department of Biology, University of Fribourg, Fribourg, Switzerland.
  5. Richard D Fetter: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.
  6. Casey M Schneider-Mizell: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States. ORCID
  7. James W Truman: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.
  8. Marta Zlatic: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.
  9. Albert Cardona: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States. ORCID
  10. Simon G Sprecher: Department of Biology, University of Fribourg, Fribourg, Switzerland. ORCID
PMID: 30726702 DOI: 10.7554/eLife.28387

Abstract

Visual systems transduce, process and transmit light-dependent environmental cues. Computation of visual features depends on photoreceptor neuron types (PR) present, organization of the eye and wiring of the underlying neural circuit. Here, we describe the circuit architecture of the visual system of larvae by mapping the synaptic wiring diagram and neurotransmitters. By contacting different targets, the two larval PR-subtypes create two converging pathways potentially underlying the computation of ambient light intensity and temporal light changes already within this first visual processing center. Locally processed visual information then signals via dedicated projection interneurons to higher brain areas including the lateral horn and mushroom body. The stratified structure of the larval optic neuropil (LON) suggests common organizational principles with the adult fly and vertebrate visual systems. The complete synaptic wiring diagram of the LON paves the way to understanding how circuits with reduced numerical complexity control wide ranges of behaviors.

Keywords

D. melanogaster Drosophila connectome neural circuit neuroscience sensory processing visual system

References

  1. Microsc Res Tech. 1999 Apr 15;45(2):65-79 [PMID: 10332725]
  2. Curr Biol. 2001 Nov 27;11(23):R986-96 [PMID: 11728329]
  3. Development. 2002 Mar;129(6):1443-53 [PMID: 11880353]
  4. J Comp Neurol. 2002 Nov 11;453(2):157-67 [PMID: 12373781]
  5. J Neurophysiol. 2004 Feb;91(2):912-23 [PMID: 14534288]
  6. J Exp Biol. 2004 Jan;207(Pt 1):179-88 [PMID: 14638844]
  7. J Comp Neurol. 2005 Jan 17;481(3):266-75 [PMID: 15593374]
  8. Neuron. 2005 Jan 20;45(2):293-300 [PMID: 15664180]
  9. Neuron. 2005 Jul 7;47(1):115-27 [PMID: 15996552]
  10. Dev Biol. 2005 Oct 15;286(2):549-58 [PMID: 16168982]
  11. J Neurosci. 2005 Oct 5;25(40):9069-79 [PMID: 16207866]
  12. Curr Biol. 2005 Oct 25;15(20):1847-54 [PMID: 16243032]
  13. Curr Biol. 2005 Dec 6;15(23):2086-96 [PMID: 16332533]
  14. Gene Expr Patterns. 2006 Mar;6(3):299-309 [PMID: 16378756]
  15. Gene Expr Patterns. 2007 Apr;7(5):584-95 [PMID: 17300994]
  16. Annu Rev Neurosci. 2007;30:505-33 [PMID: 17506643]
  17. Nat Rev Genet. 2007 Jun;8(6):450-61 [PMID: 17510665]
  18. Dev Neurobiol. 2007 Sep 1;67(10):1267-88 [PMID: 17638381]
  19. J Comp Neurol. 2007 Nov 1;505(1):32-45 [PMID: 17729267]
  20. Neural Dev. 2007 Oct 24;2:20 [PMID: 17958902]
  21. J Comp Neurol. 2008 May 1;508(1):131-52 [PMID: 18302156]
  22. Nature. 2008 Apr 24;452(7190):956-60 [PMID: 18344978]
  23. Nature. 2008 Jul 24;454(7203):533-7 [PMID: 18594514]
  24. Neuron. 2008 Jul 10;59(1):110-24 [PMID: 18614033]
  25. Bioessays. 2008 Oct;30(10):980-93 [PMID: 18800378]
  26. Neuron. 2008 Oct 23;60(2):328-42 [PMID: 18957224]
  27. J Biol Chem. 2009 Feb 27;284(9):5717-22 [PMID: 19126545]
  28. Biochem Biophys Res Commun. 2009 May 1;382(2):395-9 [PMID: 19285485]
  29. Bioinformatics. 2009 Aug 1;25(15):1984-6 [PMID: 19376822]
  30. Proc Natl Acad Sci U S A. 2009 Jun 23;106(25):10314-9 [PMID: 19502424]
  31. PLoS One. 2009 Jun 12;4(6):e5897 [PMID: 19521527]
  32. BMC Neurosci. 2009 Jun 23;10:66 [PMID: 19549295]
  33. J Neurogenet. 2009;23(4):366-77 [PMID: 19863268]
  34. J Comp Neurol. 2010 Feb 1;518(3):292-304 [PMID: 19941354]
  35. Neuron. 2010 Apr 15;66(1):15-36 [PMID: 20399726]
  36. Neuron. 2010 Apr 29;66(2):287-99 [PMID: 20435004]
  37. Nat Neurosci. 2010 Aug;13(8):973-8 [PMID: 20622873]
  38. Nature. 2010 Nov 11;468(7321):300-4 [PMID: 21068841]
  39. PLoS Comput Biol. 2011 Feb 03;7(2):e1001066 [PMID: 21304930]
  40. J Neurosci. 2011 Apr 27;31(17):6527-34 [PMID: 21525293]
  41. Neuron. 2011 Jun 23;70(6):1165-77 [PMID: 21689602]
  42. Dev Biol. 2011 Oct 1;358(1):33-43 [PMID: 21781960]
  43. Science. 2011 Sep 9;333(6048):1458-62 [PMID: 21903815]
  44. Behav Neurosci. 2011 Dec;125(6):921-9 [PMID: 21967373]
  45. Neuron. 2011 Nov 17;72(4):602-15 [PMID: 22099462]
  46. J Comp Neurol. 2012 Nov 1;520(16):3764-85 [PMID: 22627970]
  47. Nat Methods. 2012 Jun 10;9(7):717-20 [PMID: 22688414]
  48. PLoS One. 2012;7(10):e47518 [PMID: 23082175]
  49. Nat Commun. 2012;3:1156 [PMID: 23093193]
  50. Curr Biol. 2012 Dec 18;22(24):2294-302 [PMID: 23142045]
  51. Curr Biol. 2013 Feb 4;23(3):185-95 [PMID: 23333312]
  52. Proc Natl Acad Sci U S A. 2013 Jun 18;110(25):10294-9 [PMID: 23729809]
  53. Nature. 2013 Aug 8;500(7461):175-81 [PMID: 23925240]
  54. Science. 2013 Sep 6;341(6150):1113-6 [PMID: 24009394]
  55. Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):E3868-77 [PMID: 24043822]
  56. PLoS Genet. 2013;9(12):e1004027 [PMID: 24385925]
  57. J Comp Physiol A. 1987 Aug;161(2):201-13 [PMID: 2442380]
  58. J Neurosci. 2014 Feb 5;34(6):2254-63 [PMID: 24501364]
  59. FEBS Lett. 1989 Jan 30;243(2):337-42 [PMID: 2465185]
  60. Curr Biol. 2014 May 5;24(9):976-83 [PMID: 24704075]
  61. J Comp Neurol. 2014 Oct 15;522(15):3485-500 [PMID: 24752702]
  62. Curr Biol. 2014 May 19;24(10):1062-70 [PMID: 24768048]
  63. Elife. 2014 May 27;3:null [PMID: 24867217]
  64. Nature. 2014 Aug 28;512(7515):427-30 [PMID: 25043016]
  65. Development. 1989 Apr;105(4):739-46 [PMID: 2513178]
  66. Nat Neurosci. 2015 Jan;18(1):56-65 [PMID: 25485755]
  67. Proc Natl Acad Sci U S A. 2015 Jan 13;112(2):E220-9 [PMID: 25550513]
  68. Curr Biol. 2015 Feb 16;25(4):467-72 [PMID: 25619767]
  69. Nature. 2015 Apr 30;520(7549):633-9 [PMID: 25896325]
  70. Elife. 2015 May 06;4:null [PMID: 25945916]
  71. Biochem Biophys Res Commun. 2015 Jul 10;462(4):358-64 [PMID: 25964087]
  72. Elife. 2015 May 14;4:null [PMID: 25974217]
  73. Elife. 2015 Jun 10;4:e08069 [PMID: 26061864]
  74. Elife. 2015 Jun 16;4:null [PMID: 26077825]
  75. Nat Neurosci. 2015 Aug;18(8):1067-76 [PMID: 26120965]
  76. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2015 Oct;201(10):1019-27 [PMID: 26265464]
  77. Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):13711-6 [PMID: 26483464]
  78. J Neurobiol. 1989 Jul;20(5):276-94 [PMID: 2664074]
  79. Dev Biol. 2016 Feb 15;410(2):164-177 [PMID: 26769100]
  80. J Comp Neurol. 2016 Jun 15;524(9):1920-56 [PMID: 26780543]
  81. Front Physiol. 2016 Feb 25;7:46 [PMID: 26941647]
  82. Development. 2016 Apr 15;143(8):1413-23 [PMID: 26952983]
  83. Neural Plast. 2016;2016:7291438 [PMID: 26989517]
  84. Elife. 2016 Mar 18;5:null [PMID: 26990779]
  85. Elife. 2016 May 13;5: [PMID: 27177418]
  86. Cell. 2016 Oct 20;167(3):858-870.e19 [PMID: 27720450]
  87. Curr Biol. 2016 Oct 24;26(20):R1062-R1072 [PMID: 27780048]
  88. Elife. 2016 Nov 15;5: [PMID: 27845623]
  89. Elife. 2016 Dec 28;5: [PMID: 28029094]
  90. Cell Rep. 2017 Apr 4;19(1):72-85 [PMID: 28380364]
  91. Front Behav Neurosci. 2017 Apr 20;11:66 [PMID: 28473759]
  92. Elife. 2017 May 22;6: [PMID: 28530904]
  93. Nature. 2017 Aug 9;548(7666):175-182 [PMID: 28796202]
  94. J Neurosci. 1995 Aug;15(8):5623-36 [PMID: 7643206]
  95. Dev Biol. 1976 Oct 15;53(2):217-40 [PMID: 825400]
  96. Cell Tissue Res. 1993 Sep;273(3):583-98 [PMID: 8402833]
  97. Cell Tissue Res. 1995 Nov;282(2):193-202 [PMID: 8565051]
  98. J Neurogenet. 1995 Nov;10(2):119-35 [PMID: 8592272]
  99. J Comp Neurol. 1997 Apr 14;380(3):335-54 [PMID: 9087517]
  100. J Neurosci. 1997 Sep 1;17(17):6745-60 [PMID: 9254686]
  101. Behav Brain Res. 1997 Aug;87(1):1-14 [PMID: 9331469]
  102. J Neurosci. 1998 Jun 15;18(12):4673-83 [PMID: 9614242]

Grants

  1. 31003A_169993/Bundesbehörden der Schweizerischen Eidgenossenschaft
  2. ERC-2012-StG 309832-PhotoNaviNet/Seventh Framework Programme
Journal Article
Article has an altmetric score of 40

Word Cloud

Created with Highcharts 10.0.0visualcircuitwiringlarvalsystemsunderlyingneuralsystemsynapticdiagramtwolightprocessingLONVisualtransduceprocesstransmitlight-dependentenvironmentalcuesComputationfeaturesdependsphotoreceptorneurontypesPRpresentorganizationeyedescribearchitecturelarvaemappingneurotransmitterscontactingdifferenttargetsPR-subtypescreateconvergingpathwayspotentiallycomputationambientintensitytemporalchangesalreadywithinfirstcenterLocallyprocessedinformationsignalsviadedicatedprojectioninterneuronshigherbrainareasincludinglateralhornmushroombodystratifiedstructureopticneuropilsuggestscommonorganizationalprinciplesadultflyvertebratecompletepaveswayunderstandingcircuitsreducednumericalcomplexitycontrolwiderangesbehaviorsOrganizationDmelanogasterDrosophilaconnectomeneurosciencesensory

Similar Articles

Cited By