Sidekick 2 directs formation of a retinal circuit that detects differential motion

Nature

Volumn 524, Issue 7566, 2015, Pages 466-470

  Krishnaswamy, Arjun ^a   Yamagata, Masahito ^a   Duan, Xin ^a   Hong, Y Kate ^a,b   Sanes, Joshua R ^a  

^a HARVARD UNIVERSITY   (United States)

^b Howard Hughes Medical Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; IMMUNOGLOBULIN; SIDEKICK 2 PROTEIN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 3; IMMUNOGLOBULIN G; MEMBRANE PROTEIN; SDK2 PROTEIN, MOUSE;

ANTIBODY; BRAIN; CELLS AND CELL COMPONENTS; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNE SYSTEM; METABOLISM; NEUROLOGY; PHOTORECEPTION; RODENT; SENSORY SYSTEM;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MOTION; CONTROLLED STUDY; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; GAIN OF FUNCTION MUTATION; GAP JUNCTION; INTERNEURON; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RECEPTIVE FIELD; RETINA AMACRINE CELL; RETINA GANGLION CELL; SYNAPSE; ANIMAL; CYTOLOGY; FEMALE; GENETICS; MALE; METABOLISM; MOTION; MOVEMENT PERCEPTION; MUTATION; PHYSIOLOGY; VISUAL SYSTEM;

MAMMALIA;

AMACRINE CELLS; ANIMALS; FEMALE; IMMUNOGLOBULIN G; MALE; MEMBRANE PROTEINS; MICE; MOTION; MOTION PERCEPTION; MUTATION; RETINAL GANGLION CELLS; SYNAPSES; VISUAL PATHWAYS;

EID: 84940569590     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14682     Document Type: Article

References (53)

1. Sanes, J. R. & Zipursky, S. L. Design principles of insect and vertebrate visual systems. Neuron 66, 15-36 (2010).
2. Gollisch, T. & Meister, M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65, 150-164 (2010).
3. Masland, R. H. The neuronal organization of the retina. Neuron 76, 266-280 (2012).
4. Sanes, J. R. & Masland, R. H. The types of retinal ganglion cells: current status and implications for neuronal classification. Annu. Rev. Neurosci. 38, 221-246 (2015).
5. Kim, I. J., Zhang, Y., Meister, M. & Sanes, J. R. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J. Neurosci. 30, 1452-1462 (2010).
6. Zhang, Y., Kim, I. J., Sanes, J.R. & Meister, M. Themost numerous ganglion cell type of the mouse retina is a selective feature detector. Proc. Natl Acad. Sci. USA 109, E2391-E2398 (2012).
7. Baccus, S. A., Olveczky, B. P., Manu, M. & Meister, M. A retinal circuit that computes object motion. J. Neurosci. 28, 6807-6817 (2008).
8. Ölveczky, B. P., Baccus, S. A. & Meister, M. Segregation of object and background motion in the retina. Nature 423, 401-408 (2003).
9. Venkataramani, S. et al. Distinct roles for inhibition in spatial and temporal tuning of local edge detectors in the rabbit retina. PLoS ONE 9, e88560 (2014).
10. Russell, T. L. & Werblin, F. S. Retinal synaptic pathways underlying the response of the rabbit local edge detector. J. Neurophysiol. 103, 2757-2769 (2010).
11. van Wyk, M., Taylor, W. R. & Vaney, D. I. Local edge detectors: a substrate for fine spatial vision at low temporal frequencies in rabbit retina. J. Neurosci. 26, 13250-13263 (2006).
12. Levick, W. R. Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina. J. Physiol. (Lond.) 188, 285-307 (1967).
13. Yamagata, M., Weiner, J. A. & Sanes, J. R. Sidekicks: synaptic adhesionmolecules that promote lamina-specific connectivity in the retina. Cell 110, 649-660 (2002).
14. Yamagata, M. & Sanes, J. R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451, 465-469 (2008).
15. Yamagata, M. & Sanes, J. R. Synaptic localization and function of Sidekick recognition molecules require MAGI scaffolding proteins. J. Neurosci. 30, 3579-3588 (2010).
16. Haverkamp, S. & Wassle, H. Characterization of an amacrine cell type of the mammalian retina immunoreactive for vesicular glutamate transporter 3. J. Comp. Neurol. 468, 251-263 (2004).
17. Grimes, W. N., Seal, R. P., Oesch, N., Edwards, R. H. & Diamond, J. S. Genetic targeting and physiological features of VGLUT31 amacrine cells. Vis. Neurosci. 28, 381-392 (2011).
18. Johnson, J. et al. Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retina. J. Comp. Neurol. 477, 386-398 (2004).
19. Lee, S. et al. An unconventional glutamatergic circuit in the retina formed by vGluT3 amacrine cells. Neuron 84, 708-715 (2014).
20. Kim, T., Soto F. & Kerschensteiner D. An excitatory amacrine cell detects object motion and provides feature-selective input to ganglion cells in themouse retina. eLife http://dx.doi.org/10.7554/eLife.08025 (2015).
21. El Mestikawy, S. et al. From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nature Rev. Neurosci. 12, 204-216 (2011).
22. Peters, A. & Feldman, M. L. The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. I. General description. J. Neurocytol. 5, 63-84 (1976).
23. Stepanyants, A. & Chklovskii, D. B. Neurogeometry and potential synaptic connectivity. Trends Neurosci. 28, 387-394 (2005).
24. Shepherd, G. M., Stepanyants, A., Bureau, I., Chklovskii, D. & Svoboda, K. Geometric and functional organization of cortical circuits. Nature Neurosci. 8, 782-790 (2005).
25. Binzegger, T., Douglas, R. J. & Martin, K. A. A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24, 8441-8453 (2004).
26. Duan, X., Krishnaswamy, A., De la Huerta, I., Sanes, J. R. & Type, I. I. Cadherins guide assembly of a direction-selective retinal circuit. Cell 158, 793-807 (2014).
27. Matsuoka, R. L. et al. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470, 259-263 (2011).
28. Yamagata, M. & Sanes, J. R. Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J. Neurosci. 32, 14402-14414 (2012).
29. Fuerst, P. G., Koizumi, A., Masland, R. H. & Burgess, R. W. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451, 470-474 (2008).
30. Chan, W. et al. A recombineering based approach for high-throughput conditional knockout targeting vector construction. Nucleic Acids Res. 35, e64 (2007).
31. Rodríguez, C. I. et al. High-efficiency deleter mice showthatFLPe is analternative to Cre-loxP. Nature Genet. 25, 139-140 (2000).
32. Buffelli, M. et al. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424, 430-434 (2003).
33. Kay, J. N. et al. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J. Neurosci. 31, 7753-7762 (2011).
34. Duan, X. et al. Subtype-specific regeneration of retinal ganglion cells following axotomy: effects of osteopontin and mTOR signaling. Neuron 85, 1244-1256 (2015).
35. Goebbels, S. et al. Cre/loxP-mediated inactivation of the bHLHtranscription factor gene NeuroD/BETA2. Genesis 42, 247-252 (2005).
36. Kay, J.N., Voinescu, P. E., Chu, M. W. & Sanes, J.R. Neurod6 expression defines new retinal amacrine cell subtypes and regulates their fate. Nature Neurosci. 14, 965-972 (2011).
37. Zhuang, X., Masson, J., Gingrich, J. A., Rayport, S. & Hen, R. Targeted gene expression in dopamine and serotonin neurons of the mouse brain. J. Neurosci. Methods 143, 27-32 (2005).
38. Rossi, J. et al. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab. 13, 195-204 (2011).
39. Trenholm, S., Johnson, K., Li, X., Smith, R. G. & Awatramani, G. B. Parallel mechanisms encode direction in the retina. Neuron 71, 683-694 (2011).
40. Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for lightinduced activation and silencing. Nature Neurosci. 15, 793-802 (2012).
41. Buch, T. et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nature Methods 2, 419-426 (2005).
42. Dymecki, S. M., Ray, R. S. & Kim, J. C. Mapping cell fate and function using recombinase-based intersectional strategies. Methods Enzymol. 477, 183-213 (2010).
43. Furuta, Y., Lagutin, O., Hogan, B. L. & Oliver, G. C. Retina- and ventral forebrainspecificCre recombinase activity in transgenic mice. Genesis 26, 130-132(2000).
44. Yamagata, M. & Sanes, J. R. Transgenic strategy for identifying synaptic connections in mice by fluorescence complementation (GRASP). Front. Mol. Neurosci. 5, 18 (2012).
45. Lefebvre, J. L., Kostadinov, D., Chen, W. V., Maniatis, T. & Sanes, J.R. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488, 517-521 (2012).
46. Cuntz, H., Forstner, F., Borst, A. & Häusser, M. One rule to grow themall: a general theory of neuronal branching and its practical application. PLOS Comput. Biol. 6, e1000877 (2010).
47. Asari, H. & Meister, M. The projective field of retinal bipolar cells and itsmodulation by visual context. Neuron 81, 641-652 (2014).
48. Rickgauer, J. P. & Tank, D. W. Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl Acad. Sci. USA 106, 15025-15030 (2009).
49. Prakash, R. et al. Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nature Methods 9, 1171-1179 (2012).
50. Andrasfalvy, B. K., Zemelman, B. V., Tang, J. & Vaziri, A. Two-photon single-cell optogenetic control of neuronal activity by sculpted light. Proc. Natl Acad. Sci. USA 107, 11981-11986 (2010).
51. Katz, B. & Miledi, R. The release of acetylcholine from nerve endings by graded electric pulses. Proc. R. Soc. Lond. 167, 23-38 (1967).
52. Euler, T. et al. Eyecup scope-optical recordings of light stimulus-evoked fluorescence signals in the retina. Pflugers Arch. 457, 1393-1414 (2009).
53. Borghuis, B. G., Looger, L. L., Tomita, S. & Demb, J. B. Kainate receptors mediate signaling in both transient and sustained OFF bipolar cell pathways in mouse retina. J. Neurosci. 34, 6128-6139 (2014).