Spikes and ribbon synapses in early vision

Trends in Neurosciences

Volumn 36, Issue 8, 2013, Pages 480-488

  Baden, Tom ^a   Euler, Thomas ^a   Weckström, Matti ^b   Lagnado, Leon ^c,d  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF OULU   (Finland)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Action potential; Analog to digital conversion; Bipolar cell; Retina; Ribbon synapse; Spike

Indexed keywords

COMPOUND EYE; HUMAN; HYPERPOLARIZATION; INFORMATION PROCESSING; NERVE CELL MEMBRANE POTENTIAL; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; OSCILLATION; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA BIPOLAR GANGLION CELL; RETINA RECEPTIVE FIELD; REVIEW; SPIKE; SYNAPSE; VISION; VISUAL INFORMATION; VISUAL STIMULATION; VISUAL SYSTEM;

ACTION POTENTIAL; ANALOG-TO-DIGITAL CONVERSION; BIPOLAR CELL; RETINA; RIBBON SYNAPSE; SPIKE;

ACTION POTENTIALS; ANIMALS; MODELS, NEUROLOGICAL; RETINAL BIPOLAR CELLS; SYNAPSES; VISUAL PATHWAYS;

EID: 84881029884     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2013.04.006     Document Type: Review

References (105)

1. Wässle H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 2004, 5:747-757.
2. Masland R.H. The neuronal organization of the retina. Neuron 2012, 76:266-280.
3. Bloomfield S.A. Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. J. Neurophysiol. 1992, 68:711-725.
4. Wässle H., Boycott B.B. Functional architecture of the mammalian retina. Phys. Rev. 1991, 71:447-480.
5. Masland R.H. Processing and encoding of visual information in the retina. Curr. Opin. Neurobiol. 1996, 6:467-474.
6. Protti D.A., et al. Light evokes Ca2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 2000, 25:215-227.
7. Cui J., Pan Z.H. Two types of cone bipolar cells express voltage-gated Na+ channels in the rat retina. Vis. Neurosci. 2008, 25:635-645.
8. Dreosti E., et al. In vivo evidence that retinal bipolar cells generate spikes modulated by light. Nat. Neurosci. 2011, 14:951-952.
9. Baden T., et al. Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr. Biol. 2011, 21:1859-1869.
10. Saszik S., DeVries S.H. A mammalian retinal bipolar cell uses both graded changes in membrane voltage and all-or-nothing Na+ spikes to encode light. J. Neurosci. 2012, 32:297-307.
11. Juusola M., et al. Information processing by graded-potential transmission through tonically active synapses. Trends Neurosci. 1996, 19:292-297.
12. Borst A., Haag J. Neural networks in the cockpit of the fly. J. Comp. Physiol. A 2002, 188:419-437.
13. Egelhaaf M. Fly vision: neural mechanisms of motion computation. Curr. Biol. 2008, 18:R339-R341.
14. Fain G.L., et al. Phototransduction and the evolution of photoreceptors. Curr. Biol. 2010, 20:R114-R124.
15. Douglass J.K., Strausfeld N.J. Visual motion-detection circuits in flies: parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate. J. Neurosci. 1996, 16:4551-4562.
16. Uusitalo R.O., et al. Graded responses and spiking properties of identified first-order visual interneurons of the fly compound eye. J. Neurophysiol. 1995, 73:1782-1792.
17. Simmons P.J., van Steveninck R.R. Sparse but specific temporal coding by spikes in an insect sensory-motor ocellar pathway. J. Exp. Biol. 2010, 213:2629-2639.
18. Zheng L., et al. Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. J. Gen. Physiol. 2006, 127:495-510.
19. Sterling P., Matthews G. Structure and function of ribbon synapses. Trends Neurosci. 2005, 28:20-29.
20. Moser T., et al. Hair cell ribbon synapses. Cell Tissue Res. 2006, 326:347-359.
21. Nouvian R., et al. Structure and function of the hair cell ribbon synapse. J. Membr. Biol. 2006, 209:153-165.
22. LoGiudice L., Matthews G. The role of ribbons at sensory synapses. Neuroscientist 2009, 15:380-391.
23. Safieddine S., et al. The auditory hair cell ribbon synapse: from assembly to function. Annu. Rev. Neurosci. 2012, 35:509-528.
24. Prokop A., Meinertzhagen I.A. Development and structure of synaptic contacts in Drosophila. Semin. Cell Dev. Biol. 2006, 17:20-30.
25. Baylor D.A., Fuortes M.G. Electrical responses of single cones in the retina of the turtle. J. Physiol. 1970, 207:77-92.
26. Maricq A.V., Korenbrot J.I. Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1988, 1:503-515.
27. Kawai F., et al. Suppression by an h current of spontaneous Na+ action potentials in human cone and rod photoreceptors. Invest. Ophthalmol. Vis. Sci. 2005, 46:390-397.
28. Fain G.L., et al. Calcium spikes in toad rods. J. Physiol. 1980, 303:495-513.
29. Schnapf J.L., et al. Visual transduction in cones of the monkey Macaca fascicularis. J. Physiol. 1990, 427:681-713.
30. Kawai F., et al. Na(+) action potentials in human photoreceptors. Neuron 2001, 30:451-458.
31. Wei T., et al. Light-driven calcium signals in mouse cone photoreceptors. J. Neurosci. 2012, 32:6981-6994.
32. Burrone J., Lagnado L. Electrical resonance and Ca2+ influx in the synaptic terminal of depolarizing bipolar cells from the goldfish retina. J. Physiol. 1997, 505:571-584.
33. Zenisek D., Matthews G. Calcium action potentials in retinal bipolar neurons. Vis. Neurosci. 1998, 15:69-75.
34. Sakaba T., et al. Ca2+-activated K+ current at presynaptic terminals of goldfish retinal bipolar cells. Neurosci. Res. 1997, 27:219-228.
35. Ma Y.P., et al. Heterogeneous expression of voltage-dependent Na+ and K+ channels in mammalian retinal bipolar cells. Vis. Neurosci. 2005, 22:119-133.
36. Zenisek D., et al. Voltage-dependent sodium channels are expressed in nonspiking retinal bipolar neurons. J. Neurosci. 2001, 21:4543-4550.
37. Pan Z.H., Hu H.J. Voltage-dependent Na(+) currents in mammalian retinal cone bipolar cells. J. Neurophysiol. 2000, 84:2564-2571.
38. Ichinose T., et al. Sodium channels in transient retinal bipolar cells enhance visual responses in ganglion cells. J. Neurosci. 2005, 25:1856-1865.
39. Baden T., et al. Spikes in Mammalian bipolar cells support temporal layering of the inner retina. Curr. Biol. 2013, 23:48-52.
40. Baumann F. Slow and spike potentials recorded from retinula cells of the honeybee drone in response to light. J. Gen. Physiol. 1968, 52:855-875.
41. Heimonen K., et al. Large functional variability in cockroach photoreceptors: optimization to low light levels. J. Neurosci. 2006, 26:13454-13462.
42. Heimonen K., et al. Signal coding in cockroach photoreceptors is tuned to dim environments. J. Neurophysiol. 2012, 108:2641-2652.
43. Weckström M., et al. Presynaptic enhancement of signal transients in photoreceptors terminals in the compound eye. Proc. R. Soc. Lond. B 1992, 250:83-89.
44. van Hateren J.H., Laughlin S.B. Membrane parameters, signal transmission, and the design of a graded potential neuron. J. Comp. Physiol. A 1990, 166:437-448.
45. Simmons P.J. Signal processing in a simple visual system: the locust ocellar system and its synapses. Microsc. Res. Tech. 2002, 56:270-280.
46. Mennerick S., Matthews G. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 1996, 17:1241-1249.
47. Palmer M.J. Modulation of Ca(2+)-activated K+ currents and Ca(2+)-dependent action potentials by exocytosis in goldfish bipolar cell terminals. J. Physiol. 2006, 572:747-762.
48. Holt M., et al. High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr. Biol. 2004, 14:173-183.
49. Matthews G., Fuchs P. The diverse roles of ribbon synapses in sensory neurotransmission. Nat. Rev. Neurosci. 2010, 11:812-822.
50. Lenzi D., et al. Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J. Neurosci. 1999, 19:119-132.
51. Gomis A., et al. Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J. Neurosci. 1999, 19:6309-6317.
52. Singer J.H., et al. Coordinated multivesicular release at a mammalian ribbon synapse. Nat. Neurosci. 2004, 7:826-833.
53. Palmer M.J. Characterisation of bipolar cell synaptic transmission in goldfish retina using paired recordings. J. Physiol. 2010, 588:1489-1498.
54. Uusitalo R.O., Weckström M. Potentiation in the first visual synapse of the fly compound eye. J. Neurophysiol. 2000, 83:2103-2112.
55. van Steveninck R.R.R., Laughlin S.B. The rate of information transfer at graded-potential synapses. Nature 1996, 379:642-645.
56. Kretzberg J., et al. Neural coding with graded membrane potential changes and spikes. J. Comput. Neurosci. 2001, 11:153-164.
57. Meister M., Berry M.J. The neural code of the retina. Neuron 1999, 22:435-450.
58. Field G.D., Rieke F. Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 2002, 34:773-785.
59. Gollisch T., Meister M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 2010, 65:150-164.
60. Demb J.B., et al. Functional circuitry of the retinal ganglion cell's nonlinear receptive field. J. Neurosci. 1999, 19:9756-9767.
61. Brown S.P., et al. Receptive field microstructure and dendritic geometry of retinal ganglion cells. Neuron 2000, 27:371-383.
62. Petrusca D., et al. Identification and characterization of a Y-like primate retinal ganglion cell type. J. Neurosci. 2007, 27:11019-11027.
63. Schwartz G.W., et al. The spatial structure of a nonlinear receptive field. Nat. Neurosci. 2012, 15:1572-1580.
64. Roska B., Werblin F. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 2001, 410:583-587.
65. Zhang Y., et al. The most numerous ganglion cell type of the mouse retina is a selective feature detector. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E2391-E2398.
66. Fettiplace R., Fuchs P.A. Mechanisms of hair cell tuning. Annu. Rev. Physiol. 1999, 61:809-834.
67. Rutherford M.A., Roberts W.M. Spikes and membrane potential oscillations in hair cells generate periodic afferent activity in the frog sacculus. J. Neurosci. 2009, 29:10025-10037.
68. DeVries S.H., Schwartz E.A. Kainate receptors mediate synaptic transmission between cones and 'Off' bipolar cells in a mammalian retina. Nature 1999, 397:157-160.
69. Awatramani G.B., Slaughter M.M. Origin of transient and sustained responses in ganglion cells of the retina. J. Neurosci. 2000, 20:7087-7095.
70. DeVries S.H. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 2000, 28:847-856.
71. DeVries S.H., et al. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 2006, 50:735-748.
72. Puller C., et al. OFF bipolar cells express distinct types of dendritic glutamate receptors in the mouse retina. Neuroscience 2013, 10.1016/j.neuroscience.2013.03.054.
73. Abou Tayoun A.N., et al. The Drosophila SK channel (dSK) contributes to photoreceptor performance by mediating sensitivity control at the first visual network. J. Neurosci. 2011, 31:13897-13910.
74. Laughlin S.B., et al. The metabolic cost of neural information. Nat. Neurosci. 1998, 1:36-41.
75. Attwell D., Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 2001, 21:1133-1145.
76. Beckers U., et al. Precise timing in fly motion vision is mediated by fast components of combined graded and spike signals. Neuroscience 2009, 160:639-650.
77. Vallet A.M., et al. Membrane conductances involved in amplification of small signals by sodium channels in photoreceptors of drone honey bee. J. Physiol. 1992, 456:303-324.
78. Berry R.P., et al. Ocellar adaptations for dim light vision in a nocturnal bee. J. Exp. Biol. 2011, 214:1283-1293.
79. Castellano-Munoz M., et al. Efferent control of the electrical and mechanical properties of hair cells in the bullfrog's sacculus. PLoS ONE 2010, 5:e13777.
80. Marcotti W., et al. Sodium and calcium currents shape action potentials in immature mouse inner hair cells. J. Physiol. 2003, 552:743-761.
81. tom Dieck S., Brandstätter J.H. Ribbon synapses of the retina. Cell Tissue Res. 2006, 326:339-346.
82. Mercer A.J., Thoreson W.B. The dynamic architecture of photoreceptor ribbon synapses: cytoskeletal, extracellular matrix, and intramembrane proteins. Vis. Neurosci. 2011, 28:453-471.
83. Thoreson W.B. Kinetics of synaptic transmission at ribbon synapses of rods and cones. Mol. Neurobiol. 2007, 36:205-223.
84. Rieke F., Schwartz E.A. Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J. Physiol. 1996, 493(Pt 1):1-8.
85. Rabl K., et al. Kinetics of exocytosis is faster in cones than in rods. J. Neurosci. 2005, 25:4633-4640.
86. Thoreson W.B., et al. A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 2004, 42:595-605.
87. Jackman S.L., et al. Role of the synaptic ribbon in transmitting the cone light response. Nat. Neurosci. 2009, 12:303-310.
88. Innocenti B., Heidelberger R. Mechanisms contributing to tonic release at the cone photoreceptor ribbon synapse. J. Neurophysiol. 2008, 99:25-36.
89. Bartoletti T.M., et al. Vesicle pool size at the salamander cone ribbon synapse. J. Neurophysiol. 2010, 103:419-423.
90. Berntson A., Taylor W.R. The unitary event amplitude of mouse retinal on-cone bipolar cells. Vis. Neurosci. 2003, 20:621-626.
91. Choi S.Y., et al. Encoding light intensity by the cone photoreceptor synapse. Neuron 2005, 48:555-562.
92. Llobet A., et al. Exocytosis at the ribbon synapse of retinal bipolar cells studied in patches of presynaptic membrane. J. Neurosci. 2003, 23:2706-2714.
93. Zenisek D., et al. Imaging calcium entry sites and ribbon structures in two presynaptic cells. J. Neurosci. 2003, 23:2538-2548.
94. Singer J.H., Diamond J.S. Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J. Neurophysiol. 2006, 95:3191-3198.
95. von Gersdorff H., Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 1994, 367:735-739.
96. von Gersdorff H., et al. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron 1996, 16:1221-1227.
97. Beaumont V., et al. Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:10700-10705.
98. Tucker T., Fettiplace R. Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells. Neuron 1995, 15:1323-1335.
99. Rutherford M.A., Roberts W.M. Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2898-2903.
100. Schnee M.E., et al. Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 2005, 47:243-254.
101. Moser T., Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:883-888.
102. Meyer A.C., et al. Tuning of synapse number, structure and function in the cochlea. Nat. Neurosci. 2009, 12:444-453.
103. Zampini V., et al. Elementary properties of CaV1.3 Ca(2+) channels expressed in mouse cochlear inner hair cells. J. Physiol. 2010, 588:187-199.
104. Meinertzhagen I.A., O'Neil S.D. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 1991, 305:232-263.
105. Fröhlich A., Meinertzhagen I.A. Quantitative features of synapse formation in the fly's visual system. I. The presynaptic photoreceptor terminal. J. Neurosci. 1983, 3:2336-2349.