Cited by 450Visual perception and processing mechanismsNeuroscience and Neuropharmacology ResearchRetinal Development and Disorders

Space–time wiring specificity supports direction selectivity in the retina

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the EyeWirers, Kim, Jinseop S., Greene, Matthew J., Zlateski, Aleksandar, Lee, Kisuk, Richardson, Mark, Turaga, Srinivas C., Purcaro, Michael +6 more·2014·Nature

Abstract

How does the mammalian retina detect motion? This classic problem in visual neuroscience has remained unsolved for 50 years. In search of clues, here we reconstruct Off-type starburst amacrine cells (SACs) and bipolar cells (BCs) in serial electron microscopic images with help from EyeWire, an online community of 'citizen neuroscientists'. On the basis of quantitative analyses of contact area and branch depth in the retina, we find evidence that one BC type prefers to wire with a SAC dendrite near the SAC soma, whereas another BC type prefers to wire far from the soma. The near type is known to lag the far type in time of visual response. A mathematical model shows how such 'space-time wiring specificity' could endow SAC dendrites with receptive fields that are oriented in space-time and therefore respond selectively to stimuli that move in the outward direction from the soma.

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  • Only players who met a certain accuracy threshold, determined by their accuracy on a previously published retinal dataset, were allowed to reconstruct zebrafish neurons.

    “only players who met a certain threshold (see below), determined by their accuracy on a previously published retinal dataset14,77, were allowed to reconstruct zebrafish neurons”

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  1. [1]Borst A Euler T Seeing things in motion: models, circuits, and mechanisms. Neuron 2011 71 974 94 21943597
  2. [2]Vaney DI Sivyer B Taylor WR Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat. Rev. Neurosci 2012 13 194 208 22314444
  3. [3]Euler T Detwiler PB Denk W Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 2002 418 845 52 12192402
  4. [4]Hausselt SE Euler T Detwiler PB Denk W A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol 2007 5 e185 17622194 PMC1906843
  5. [5]Yonehara K The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 2013 79 1078 85 23973208
  6. [6]Wässle H Puller C Müller F Haverkamp S Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. The Journal of Neuroscience 2009 29 106 117 19129389 PMC6664901
  7. [7]Baden T Berens P Bethge M Euler T Spikes in mammalian bipolar cells support temporal layering of the inner retina. Curr Biol 2013 23 48 52 23246403
  8. [8]Borghuis BG Marvin JS Looger LL Demb JB Two-photon imaging of nonlinear glutamate release dynamics at bipolar cell synapses in the mouse retina. J Neurosci 2013 33 10972 85 23825403 PMC3718381
  9. [11]Cooper S Predicting protein structures with a multiplayer online game. Nature 2010 466 756 60 20686574 PMC2956414
  10. [12]Fiala JC Reconstruct: a free editor for serial section microscopy. J Microsc 2005 218 52 61 15817063
  11. [13]Von Ahn L Dabbish L Labeling images with a computer game. Proceedings of the SIGCHI conference on human factors in computing systems 2004 319 326 ACM
  12. [14]Helmstaedter M Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 2013 500 168 74 23925239
  13. [15]Famiglietti EV Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction. J Comp Neurol 1991 309 40 70 1894768
  14. [16]Berry MJ II Meister M Refractoriness and neural precision. J Neurosci 1998 18 2200 11 9482804 PMC6792934
  15. [17]Baccus SA Meister M Fast and slow contrast adaptation in retinal circuitry. Neuron 2002 36 909 19 12467594
  16. [18]Watson AB Ahumada AJ Jr. Model of human visual-motion sensing. J Opt Soc Am A 1985 2 322 41 3973764
  17. [19]Adelson EH Bergen JR Spatiotemporal energy models for the perception of motion. J Opt Soc Am A 1985 2 284 99 3973762
  18. [21]Barlow HB Levick WR The mechanism of directionally selective units in rabbit's retina. J Physiol 1965 178 477 504 5827909 PMC1357309
  19. [22]Borst A Reisenman C Haag J Adaptation of response transients in fly motion vision. II: Model studies. Vision Res 2003 43 1309 22 12726836
  20. [23]Lagnado L Gomis A Job C Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 1996 17 957 67 8938127
  21. [24]Tukker JJ Taylor WR Smith RG Direction selectivity in a model of the starburst amacrine cell. Visual neuroscience 2004 21 611 625 15579224
  22. [26]Gavrikov KE Dmitriev AV Keyser KT Mangel SC Cation–chloride cotransporters mediate neural computation in the retina. Proc Natl Acad Sci U S A 2003 100 16047 52 14665697 PMC307690
  23. [27]Münch TA Werblin FS Symmetric interactions within a homogeneous starburst cell network can lead to robust asymmetries in dendrites of starburst amacrine cells. J Neurophysiol 2006 96 471 7 16598066
  24. [28]Lee S Zhou ZJ The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 2006 51 787 99 16982423 PMC4227911
  25. [29]Kim I-J Zhang Y Yamagata M Meister M Sanes JR Molecular identification of a retinal cell type that responds to upward motion. Nature 2008 452 478 82 18368118
  26. [30]Maisak MS A directional tuning map of drosophila elementary motion detectors. Nature 2013 500 212 6 23925246
  27. [33]Kalisman N Silberberg G Markram H Deriving physical connectivity from neuronal morphology. Biol Cybern 2003 88 210 8 12647228
  28. [34]Binzegger T Douglas RJ Martin KAC A quantitative map of the circuit of cat primary visual cortex. J Neurosci 2004 24 8441 53 15456817 PMC6729898
  29. [36]Fried SI Münch TA Werblin FS Mechanisms and circuitry underlying directional selectivity in the retina. Nature 2002 420 411 4 12459782
  30. [37]Yonehara K Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 2010 469 407 410 21170022
  31. [38]Wei W Hamby AM Zhou K Feller MB Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 2010 469 402 406 21131947 PMC3974627
  32. [40]Turaga S Briggman K Helmstaedter M Denk W Seung S Bengio Y Schuurmans D Lafferty J Williams CKI Culotta A Maximin affinity learning of image segmentation. Advances in Neural Information Processing Systems 2009 22 1865 1873
  33. [41]Turaga SC Convolutional networks can learn to generate affinity graphs for image segmentation. Neural Comput 2010 22 511 38 19922289
  34. [42]Ciresan D Giusti A Schmidhuber J Deep neural networks segment neuronal membranes in electron microscopy images. Advances in Neural Information Processing Systems 2012 25 2852 2860
  35. [43]Mutch J Knoblich U Poggio T CNS: a GPU-based framework for simulating cortically-organized networks. Tech. Rep. MIT-CSAIL-TR-2010-013 / CBCL-286 2010 Massachusetts Institute of Technology Cambridge, MA
  36. [44]Jeon C-J Strettoi E Masland RH The major cell populations of the mouse retina. J Neurosci 1998 18 8936 8946 9786999 PMC6793518

Cited by

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Authors
EyeWirers, T., Kim, J. S., Greene, M. J., Zlateski, A., Lee, K., Richardson, M., Turaga, S. C., Purcaro, M., Balkam, M., Robinson, A., Behabadi, B. F., Campos, M., Denk, W., & Seung, H. S.
Affiliations
  • Massachusetts Institute of Technology (US)
  • Qualcomm (United States) (US)
  • Max Planck Society (DE)
  • Max Planck Institute for Medical Research (DE)
Corresponding author
Seung, H. Sebastian
Venue
Nature
Published
2014-05
Volume
509
Issue
7500
Pages
331-336
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2040156859
Cited by
450
References
5
Citations by year
2026: 18 · 2025: 12 · 2024: 27 · 2023: 29 · 2022: 39 · 2021: 31 · 2020: 27 · 2019: 50 · 2018: 48 · 2017: 49 · 2016: 58 · 2015: 38 · 2014: 23
FWCI
28.67
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • National Institute of Neurological Disorders and Stroke (R01NS076467)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
Keywords
direction selectivity, motion detection, starburst amacrine cells, bipolar cells, retinal circuitry, citizen science, mouse retina, insect vision
MeSH terms
Animals, Artificial Intelligence, Brain Mapping, Dendrites, Models, Neurological, Motion, Neural Pathways, Retina, Presynaptic Terminals, Amacrine Cells, Retinal Bipolar Cells, Mice, Spatio-Temporal Analysis, Crowdsourcing

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