Retinal bipolar cells: elementary building blocks of vision (original) (raw)

• Dreosti, E., Odermatt, B., Dorostkar, M. M. & Lagnado, L. A genetically encoded reporter of synaptic activity in vivo. Nature Methods 6, 883–889 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Baden, T., Berens, P., Bethge, M. & Euler, T. Spikes in mammalian bipolar cells support temporal layering of the inner retina. Curr. Biol. 23, 48–52 (2013). A study in mice showing direct measurements of light-evoked presynaptic calcium responses in axonal terminals of bipolar cells that stratify at different depths within the IPL.
  Article CAS PubMed Google Scholar
• Yonehara, K. et al. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 79, 1078–1085 (2013). A mouse study demonstrating that direction selectivity is not a feature of bipolar cell output.
  Article CAS PubMed Google Scholar
• Marvin, J. S. et al. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nature Methods 10, 162–170 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Borghuis, B. G., Marvin, J. S., Looger, L. L. & Demb, J. B. Two-photon imaging of nonlinear glutamate release dynamics at bipolar cell synapses in the mouse retina. J. Neurosci. 33, 10972–10985 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Helmstaedter, M. et al. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500, 168–174 (2013). This paper provides a comprehensive, high-density electron microscopy-based reconstruction of a small patch of mouse retina.
  Article CAS PubMed Google Scholar
• Puthussery, T., Venkataramani, S., Gayet-Primo, J., Smith, R. G. & Taylor, W. R. NaV1.1 channels in axon initial segments of bipolar cells augment input to magnocellular visual pathways in the primate retina. J. Neurosci. 33, 16045–16059 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Tartuferi, F. Sull'anatomia della retina. Int. Monatsschrift Anat.Physiol. 4, 421–441 (in Italian) (1887).
  Google Scholar
• Lin, B. & Masland, R. H. Synaptic contacts between an identified type of ON cone bipolar cell and ganglion cells in the mouse retina. Eur. J. Neurosci. 21, 1257–1270 (2005).
  Article PubMed Google Scholar
• Morgan, J. L., Soto, F., Wong, R. O. & Kerschensteiner, D. Development of cell type-specific connectivity patterns of converging excitatory axons in the retina. Neuron 71, 1014–1021 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Neumann, S. & Haverkamp, S. Characterization of small-field bistratified amacrine cells in macaque retina labeled by antibodies against synaptotagmin-2. J. Comp. Neurol. 521, 709–724 (2013).
  Article CAS PubMed Google Scholar
• Hartveit, E. Functional organization of cone bipolar cells in the rat retina. J. Neurophysiol. 77, 1716–1730 (1997).
  Article CAS PubMed Google Scholar
• Wässle, H., Puller, C., Müller, F. & Haverkamp, S. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J. Neurosci. 29, 106–117 (2009). Key work on the anatomical identification of bipolar cell types and their organization in the mouse.
  Article PubMed PubMed Central CAS Google Scholar
• Connaughton, V. P., Graham, D. & Nelson, R. Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. J. Comp. Neurol. 477, 371–385 (2004).
  Article CAS PubMed Google Scholar
• Li, Y. N., Tsujimura, T., Kawamura, S. & Dowling, J. E. Bipolar cell-photoreceptor connectivity in the zebrafish (Danio rerio) retina. J. Comp. Neurol. 520, 3786–3802 (2012).
  Article PubMed PubMed Central Google Scholar
• Cajal, S. R.Y. La rétine des vertébrés. La Cellule 9, 119–257 (in French) (1893).
  Google Scholar
• Euler, T., Schneider, H. & Wässle, H. Glutamate responses of bipolar cells in a slice preparation of the rat retina. J. Neurosci. 16, 2934–2944 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Euler, T. & Masland, R. H. Light-evoked responses of bipolar cells in a mammalian retina. J. Neurophysiol. 83, 1817–1829 (2000).
  Article CAS PubMed Google Scholar
• Odermatt, B., Nikolaev, A. & Lagnado, L. Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron 73, 758–773 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Mataruga, A., Kremmer, E. & Muller, F. Type 3a and type 3b OFF cone bipolar cells provide for the alternative rod pathway in the mouse retina. J. Comp. Neurol. 502, 1123–1137 (2007).
  Article CAS PubMed Google Scholar
• Puller, C., Ivanova, E., Euler, T., Haverkamp, S. & Schubert, T. OFF bipolar cells express distinct types of dendritic glutamate receptors in the mouse retina. Neuroscience 243, 136–148 (2013).
  Article CAS PubMed Google Scholar
• Breuninger, T., Puller, C., Haverkamp, S. & Euler, T. Chromatic bipolar cell pathways in the mouse retina. J. Neurosci. 31, 6504–6517 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Ghosh, K. K., Bujan, S., Haverkamp, S., Feigenspan, A. & Wassle, H. Types of bipolar cells in the mouse retina. J. Comp. Neurol. 469, 70–82 (2004).
  Article PubMed Google Scholar
• Joo, H. R., Peterson, B. B., Haun, T. J. & Dacey, D. M. Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections. Vis. Neurosci. 28, 29–37 (2011).
  Article PubMed Google Scholar
• Light, A. C. et al. Organizational motifs for ground squirrel cone bipolar cells. J. Comp. Neurol. 520, 2864–2887 (2012).
  Article PubMed PubMed Central Google Scholar
• MacNeil, M. A., Heussy, J. K., Dacheux, R. F., Raviola, E. & Masland, R. H. The population of bipolar cells in the rabbit retina. J. Comp. Neurol. 472, 73–86 (2004).
  Article PubMed Google Scholar
• Baden, T. et al. A tale of two retinal domains: near-optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution. Neuron 80, 1206–1217 (2013).
  Article CAS PubMed Google Scholar
• Zhang, Y., Kim, I. J., Sanes, J. R. & Meister, M. The most numerous ganglion cell type of the mouse retina is a selective feature detector. Proc. Natl Acad. Sci. USA 109, E2391–E2398 (2012).
  CAS PubMed PubMed Central Google Scholar
• Bleckert, A., Schwartz, G. W., Turner, M. H., Rieke, F. & Wong, R. O. Visual space is represented by nonmatching topographies of distinct mouse retinal ganglion cell types. Curr. Biol. 24, 310–315 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Haverkamp, S., Haeseleer, F. & Hendrickson, A. A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina. Vis. Neurosci. 20, 589–600 (2003).
  Article PubMed Google Scholar
• Puller, C., Ondreka, K. & Haverkamp, S. Bipolar cells of the ground squirrel retina. J. Comp. Neurol. 519, 759–774 (2011).
  Article PubMed Google Scholar
• Li, W. & DeVries, S. H. Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nature Neurosci. 9, 669–675 (2006).
  Article CAS PubMed Google Scholar
• Schubert, T. et al. Development of presynaptic inhibition onto retinal bipolar cell axon terminals is subclass-specific. J. Neurophysiol. 100, 304–316 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Wassle, H., Grunert, U., Martin, P. R. & Boycott, B. B. Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Res. 34, 561–579 (1994).
  Article CAS PubMed Google Scholar
• Cuenca, N. et al. The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters. J. Neurocytol. 31, 649–666 (2002).
  Article CAS PubMed Google Scholar
• Puthussery, T., Gayet-Primo, J., Taylor, W. R. & Haverkamp, S. Immunohistochemical identification and synaptic inputs to the diffuse bipolar cell type DB1 in macaque retina. J. Comp. Neurol. 519, 3640–3656 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Connaughton, V. P. Bipolar cells in the zebrafish retina. Vis. Neurosci. 28, 77–93 (2011).
  Article CAS PubMed Google Scholar
• Pang, J. J., Gao, F. & Wu, S. M. Stratum-by-stratum projection of light response attributes by retinal bipolar cells of Ambystoma. J. Physiol. 558, 249–262 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Haverkamp, S., Mockel, W. & Ammermüller, J. Different types of synapses with different spectral types of cones underlie color opponency in a bipolar cell of the turtle retina. Vis. Neurosci. 16, 801–809 (1999).
  Article CAS PubMed Google Scholar
• Masland, R. H. The neuronal organization of the retina. Neuron 76, 266–280 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Ozuysal, Y. & Baccus, S. A. Linking the computational structure of variance adaptation to biophysical mechanisms. Neuron 73, 1002–1015 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Nikolaev, A., Leung, K. M., Odermatt, B. & Lagnado, L. Synaptic mechanisms of adaptation and sensitization in the retina. Nature Neurosci. 16, 934–941 (2013).
  Article CAS PubMed Google Scholar
• Manookin, M. B. & Demb, J. B. Presynaptic mechanism for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 50, 453–464 (2006).
  Article CAS PubMed Google Scholar
• Baden, T., Euler, T., Weckstrom, M. & Lagnado, L. Spikes and ribbon synapses in early vision. Trends Neurosci. 36, 480–488 (2013).
  Article CAS PubMed Google Scholar
• Taylor, W. R. & Smith, R. G. Trigger features and excitation in the retina. Curr. Opin. Neurobiol. 21, 672–678 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Hack, I., Peichl, L. & Brandstätter, J. H. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proc. Natl Acad. Sci. USA 96, 14130–14135 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Fyk-Kolodziej, B., Qin, P. & Pourcho, R. G. Identification of a cone bipolar cell in cat retina which has input from both rod and cone photoreceptors. J. Comp. Neurol. 464, 104–113 (2003).
  Article PubMed Google Scholar
• Haverkamp, S. et al. Type 4 OFF cone bipolar cells of the mouse retina express calsenilin and contact cones as well as rods. J. Comp. Neurol. 507, 1087–1101 (2008).
  Article CAS PubMed Google Scholar
• Li, W., Chen, S. & DeVries, S. H. A fast rod photoreceptor signaling pathway in the mammalian retina. Nature Neurosci. 13, 414–416 (2010).
  Article CAS PubMed Google Scholar
• Koike, C., Numata, T., Ueda, H., Mori, Y. & Furukawa, T. TRPM1: a vertebrate TRP channel responsible for retinal ON bipolar function. Cell Calcium 48, 95–101 (2010).
  Article CAS PubMed Google Scholar
• Regus-Leidig, H. & Brandstatter, J. H. Structure and function of a complex sensory synapse. Acta Physiol. 204, 479–486 (2012).
  Article CAS Google Scholar
• DeVries, S. H. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856 (2000).
  Article CAS PubMed Google Scholar
• Lindstrom, S. H., Ryan, D. G., Shi, J. & Devries, S. H. Kainate receptor subunit diversity underlying response diversity in retinal Off bipolar cells. J. Physiol. 592, 1457–1477 (2014). A detailed dissection of how OFF bipolar cell types (in the ground squirrel) inherit different kinetic properties based on differential expression of glutamate receptor types on their dendrites.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Masu, M. et al. Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80, 757–765 (1995).
  Article CAS PubMed Google Scholar
• Cao, Y. et al. Regulators of G protein signaling RGS7 and RGS11 determine the onset of the light response in ON bipolar neurons. Proc. Natl Acad. Sci. USA 109, 7905–7910 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Pearring, J. N. et al. A role for nyctalopin, a small leucine-rich repeat protein, in localizing the TRP melastatin 1 channel to retinal depolarizing bipolar cell dendrites. J. Neurosci. 31, 10060–10066 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Cao, Y. et al. Targeting of RGS7/Gβ5 to the dendritic tips of ON-bipolar cells is independent of its association with membrane anchor R7BP. J. Neurosci. 28, 10443–10449 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Cao, Y. et al. Retina-specific GTPase accelerator RGS11/G β 5S/R9AP is a constitutive heterotrimer selectively targeted to mGluR6 in ON-bipolar neurons. J. Neurosci. 29, 9301–9313 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Jeffrey, B. G. et al. R9AP stabilizes RGS11-G β5 and accelerates the early light response of ON-bipolar cells. Vis. Neurosci. 27, 9–17 (2010).
  Article PubMed PubMed Central Google Scholar
• Ray, T. A. et al. GPR179 is required for high sensitivity of the mGluR6 signaling cascade in depolarizing bipolar cells. J. Neurosci. 34, 6334–6343 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Sulaiman, P., Fina, M., Feddersen, R. & Vardi, N. Ret-PCP2 colocalizes with protein kinase C in a subset of primate ON cone bipolar cells. J. Comp. Neurol. 518, 1098–1112 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Xu, Y. et al. Retinal ON bipolar cells express a new PCP2 splice variant that accelerates the light response. J. Neurosci. 28, 8873–8884 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• De Sevilla Müller, L. P., Liu, J., Solomon, A., Rodriguez, A. & Brecha, N. C. Expression of voltage-gated calcium channel α2δ4 subunits in the mouse and rat retina. J. Comp. Neurol. 521, 2486–2501 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Sulaiman, P. et al. Kir2.4 surface expression and basal current are affected by heterotrimeric G-proteins. J. Biol. Chem. 288, 7420–7429 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Rampino, M. A. & Nawy, S. A. Relief of Mg2+-dependent inhibition of TRPM1 by PKCα at the rod bipolar cell synapse. J. Neurosci. 31, 13596–13603 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Morgans, C. W. et al. TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. Proc. Natl Acad. Sci. USA 106, 19174–19178 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Koike, C. et al. TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. Proc. Natl Acad. Sci. USA 107, 332–337 (2010). References 67 and 68 first showed that TRPM1 is the cation channel that lies downstream of the mGluR6 signalling cascade in mouse ON bipolar cells.
  Article CAS PubMed Google Scholar
• Gilliam, J. C. & Wensel, T. G. TRP channel gene expression in the mouse retina. Vision Res. 51, 2440–2452 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Haverkamp, S., Grünert, U. & Wässle, H. Localization of kainate receptors at the cone pedicles of the primate retina. J. Comp. Neurol. 436, 471–486 (2001).
  Article CAS PubMed Google Scholar
• Haverkamp, S., Grünert, U. & Wässle, H. The cone pedicle, a complex synapse in the retina. Neuron 27, 85–95 (2000). This study in the macaque provides a demonstration of the complexity of photoreceptor-to-bipolar cell connections.
  Article CAS PubMed Google Scholar
• DeVries, S. H., Li, W. & Saszik, S. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50, 735–748 (2006). A study in ground squirrels that provides evidence for the notion that functional differences in bipolar cell types may in part result from different contact morphologies with cones.
  Article CAS PubMed Google Scholar
• Vardi, N., Duvoisin, R., Wu, G. & Sterling, P. Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. J. Comp. Neurol. 423, 402–412 (2000).
  Article CAS PubMed Google Scholar
• Neitz, J. & Neitz, M. The genetics of normal and defective color vision. Vision Res. 51, 633–651 (2011).
  Article CAS PubMed Google Scholar
• Dacey, D. M., Crook, J. D. & Packer, O. S. Distinct synaptic mechanisms create parallel S-ON & S-OFF color opponent pathways in the primate retina. Vis. Neurosci. 31, 1–13 (2013).
  Google Scholar
• Nathans, J. The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments. Neuron 24, 299–312 (1999).
  Article CAS PubMed Google Scholar
• Wong, K. Y. & Dowling, J. E. Retinal bipolar cell input mechanisms in giant danio. III. ON-OFF bipolar cells and their color-opponent mechanisms. J. Neurophysiol. 94, 265–272 (2005).
  Article PubMed Google Scholar
• Dunn, F. A. & Wong, R. O. Diverse strategies engaged in establishing stereotypic wiring patterns among neurons sharing a common input at the visual system's first synapse. J. Neurosci. 32, 10306–10317 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, S. C. & Grünert, U. Connections of diffuse bipolar cells in primate retina are biased against S-cones. J. Comp. Neurol. 502, 126–140 (2007).
  Article CAS PubMed Google Scholar
• Mariani, A. P. Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive. Nature 308, 184–186 (1984).
  Article CAS PubMed Google Scholar
• Puller, C. & Haverkamp, S. Bipolar cell pathways for color vision in non-primate dichromats. Vis. Neurosci. 28, 51–60 (2011).
  Article PubMed Google Scholar
• Mills, S. L., Tian, L. M., Hoshi, H., Whitaker, C. M. & Massey, S. C. Three distinct blue-green color pathways in a mammalian retina. J. Neurosci. 34, 1760–1768 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Polyak, S. L. The Retina (University of Chicago Press, 1941).
  Google Scholar
• Kryger, Z., Galli-Resta, L., Jacobs, G. H. & Reese, B. E. The topography of rod and cone photoreceptors in the retina of the ground squirrel. Vis. Neurosci. 15, 685–691 (1998).
  Article CAS PubMed Google Scholar
• Thoreson, W. B. & Mangel, S. C. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 31, 407–441 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Vardi, N., Zhang, L. L., Payne, J. A. & Sterling, P. Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J. Neurosci. 20, 7657–7663 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Duebel, J. et al. Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon. Neuron 49, 81–94 (2006).
  Article CAS PubMed Google Scholar
• Miller, R. F. & Dacheux, R. F. Intracellular chloride in retinal neurons: measurement and meaning. Vision Res. 23, 399–411 (1983).
  Article CAS PubMed Google Scholar
• Gollisch, T. & Meister, M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65, 150–164 (2010). A key review that discusses how retinal feature extraction relies heavily on non-linearities in bipolar cell processing.
  Article CAS PubMed PubMed Central Google Scholar
• Schwartz, G. W. et al. The spatial structure of a nonlinear receptive field. Nature Neurosci. 15, 1572–1580 (2012). A demonstration of how comparatively simple cascade models may account for a substantial fraction of mouse RGC response variance under complex stimulation.
  Article CAS PubMed Google Scholar
• Baccus, S. A. & Meister, M. Fast and slow contrast adaptation in retinal circuitry. Neuron 36, 909–919 (2002).
  Article CAS PubMed Google Scholar
• Spruston, N., Jaffe, D. B. & Johnston, D. Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties. Trends Neurosci. 17, 161–166 (1994).
  Article CAS PubMed Google Scholar
• Sherry, D. M. & Yazulla, S. Goldfish bipolar cells and axon terminal patterns: a Golgi study. J. Comp. Neurol. 329, 188–200 (1993).
  Article CAS PubMed Google Scholar
• Baden, T. & Euler, T. Early vision: where (some of) the magic happens. Curr. Biol. 23, R1096–R1098 (2013).
  Article CAS PubMed Google Scholar
• Burrone, J. & Lagnado, L. Electrical resonance and Ca2+ influx in the synaptic terminal of depolarizing bipolar cells from the goldfish retina. J. Physiol. 505, 571–584 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Protti, D. A., Flores-Herr, N. & von Gersdorff, H. Light evokes Ca2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 25, 215–227 (2000). The first study to demonstrate that light can drive spikes in retinal bipolar cells (the study was conducted in goldfish).
  Article CAS PubMed Google Scholar
• Baden, T., Esposti, F., Nikolaev, A. & Lagnado, L. Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr. Biol. 21, 1859–1869 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Cui, J. & Pan, Z. H. Two types of cone bipolar cells express voltage-gated Na+ channels in the rat retina. Vis. Neurosci. 25, 635–645 (2008).
  Article PubMed PubMed Central Google Scholar
• 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. 32, 297–307 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Hu, H. J. & Pan, Z. H. Differential expression of K+ currents in mammalian retinal bipolar cells. Vis. Neurosci. 19, 163–173 (2002).
  Article PubMed Google Scholar
• Okada, T., Horiguchi, H. & Tachibana, M. Ca2+-dependent Cl− current at the presynaptic terminals of goldfish retinal bipolar cells. Neurosci. Res. 23, 297–303 (1995).
  Article CAS PubMed Google Scholar
• Connaughton, V. P. & Maguire, G. Differential expression of voltage-gated K+ and Ca2+ currents in bipolar cells in the zebrafish retinal slice. Eur. J. Neurosci. 10, 1350–1362 (1998).
  Article CAS PubMed Google Scholar
• Müller, F. et al. HCN channels are expressed differentially in retinal bipolar cells and concentrated at synaptic terminals. Eur. J. Neurosci. 17, 2084–2096 (2003).
  Article PubMed Google Scholar
• Euler, T. & Wässle, H. Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. J. Neurophysiol. 79, 1384–1395 (1998).
  Article CAS PubMed Google Scholar
• Eggers, E. D., McCall, M. A. & Lukasiewicz, P. D. Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. J. Physiol. 582, 569–582 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Ivanova, E., Müller, U. & Wässle, H. Characterization of the glycinergic input to bipolar cells of the mouse retina. Eur. J. Neurosci. 23, 350–364 (2006).
  Article PubMed Google Scholar
• Vigh, J., Vickers, E. & von Gersdorff, H. Light-evoked lateral GABAergic inhibition at single bipolar cell synaptic terminals is driven by distinct retinal microcircuits. J. Neurosci. 31, 15884–15893 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Masland, R. H. The tasks of amacrine cells. Vis. Neurosci. 29, 3–9 (2012).
  Article PubMed PubMed Central Google Scholar
• Esposti, F., Johnston, J., Rosa, J. M., Leung, K. M. & Lagnado, L. Olfactory stimulation selectively modulates the OFF pathway in the retina of zebrafish. Neuron 79, 97–110 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Yang, J., Pahng, J. & Wang, G. Y. Dopamine modulates the off pathway in light-adapted mouse retina. J. Neurosci. Res. 91, 138–150 (2013).
  CAS PubMed Google Scholar
• Tooker, R. E. et al. Nitric oxide mediates activity-dependent plasticity of retinal bipolar cell output via S-nitrosylation. J. Neurosci. 33, 19176–19193 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ayoub, G. S. & Matthews, G. Substance P modulates calcium current in retinal bipolar neurons. Vis. Neurosci. 8, 539–544 (1992).
  Article CAS PubMed Google Scholar
• Casini, G. et al. Expression of the neurokinin 1 receptor in the rabbit retina. Neuroscience 115, 1309–1321 (2002).
  Article CAS PubMed Google Scholar
• Zenisek, D., Davila, V., Wan, L. & Almers, W. Imaging calcium entry sites and ribbon structures in two presynaptic cells. J. Neurosci. 23, 2538–2548 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Llobet, A., Cooke, A. & Lagnado, L. Exocytosis at the ribbon synapse of retinal bipolar cells studied in patches of presynaptic membrane. J. Neurosci. 23, 2706–2714 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Singer, J. H., Lassova, L., Vardi, N. & Diamond, J. S. Coordinated multivesicular release at a mammalian ribbon synapse. Nature Neurosci. 7, 826–833 (2004).
  Article CAS PubMed Google Scholar
• Midorikawa, M., Tsukamoto, Y., Berglund, K., Ishii, M. & Tachibana, M. Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells. Nature Neurosci. 10, 1268–1276 (2007).
  Article CAS PubMed Google Scholar
• tom Dieck, S. & Brandstätter, J. H. Ribbon synapses of the retina. Cell Tissue Res. 326, 339–346 (2006).
  Article PubMed Google Scholar
• LoGiudice, L. & Matthews, G. The role of ribbons at sensory synapses. Neuroscientist 15, 380–391 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Beaumont, V., Llobet, A. & Lagnado, L. Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. Proc. Natl Acad. Sci. USA 102, 10700–10705 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Jackman, S. L. et al. Role of the synaptic ribbon in transmitting the cone light response. Nature Neurosci. 12, 303–310 (2009). Seminal work on how calcium drives release at a ribbon synapse (in lizards).
  Article CAS PubMed Google Scholar
• Sikora, M. A., Gottesman, J. & Miller, R. F. A computational model of the ribbon synapse. J. Neurosci. Methods 145, 47–61 (2005).
  Article PubMed Google Scholar
• Palmer, M. J. Modulation of Ca2+-activated K+ currents and Ca2+-dependent action potentials by exocytosis in goldfish bipolar cell terminals. J. Physiol. 572, 747–762 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Awatramani, G. B. & Slaughter, M. M. Intensity-dependent, rapid activation of presynaptic metabotropic glutamate receptors at a central synapse. J. Neurosci. 21, 741–749 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Veruki, M. L., Morkve, S. H. & Hartveit, E. Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling. Nature Neurosci. 9, 1388–1396 (2006).
  Article CAS PubMed Google Scholar
• Guerrero, G. et al. Heterogeneity in synaptic transmission along a Drosophila larval motor axon. Nature Neurosci. 8, 1188–1196 (2005).
  Article CAS PubMed Google Scholar
• Euler, T. & Denk, W. Dendritic processing. Curr. Opin. Neurobiol. 11, 415–422 (2001).
  Article CAS PubMed Google Scholar
• Baden, T. & Hedwig, B. Primary afferent depolarization and frequency processing in auditory afferents. J. Neurosci. 30, 14862–14869 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Gaudry, Q., Hong, E. J., Kain, J., de Bivort, B. L. & Wilson, R. I. Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila. Nature 493, 424–428 (2013).
  Article CAS PubMed Google Scholar
• Asari, H. & Meister, M. Divergence of visual channels in the inner retina. Nature Neurosci. 15, 1581–1589 (2012). A study in salamanders that provides the first evidence that individual bipolar cells may have different synaptic transfer functions according to the different postsynaptic partners.
  Article CAS PubMed Google Scholar
• Asari, H. & Meister, M. The projective field of retinal bipolar cells and its modulation by visual context. Neuron 81, 641–652 (2014). This study presents evidence that individual salamander bipolar cells functionally feed into an unexpectedly large number and variety of postsynaptic circuits.
  Article CAS PubMed Google Scholar
• Sumbul, U. et al. A genetic and computational approach to structurally classify neuronal types. Nature Commun. 5, 3512 (2014).
  Article CAS Google Scholar
• Sun, W., Li, N. & He, S. Large-scale morphological survey of mouse retinal ganglion cells. J. Comp. Neurol. 451, 115–126 (2002).
  Article PubMed Google Scholar
• Volgyi, B., Chheda, S. & Bloomfield, S. A. Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J. Comp. Neurol. 512, 664–687 (2009).
  Article PubMed PubMed Central Google Scholar
• Roska, B. & Werblin, F. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587 (2001). Key work in rabbits on the functional stratification rules of the IPL.
  Article CAS PubMed Google Scholar
• Awatramani, G. B. & Slaughter, M. M. Origin of transient and sustained responses in ganglion cells of the retina. J. Neurosci. 20, 7087–7095 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Field, G. D. et al. Functional connectivity in the retina at the resolution of photoreceptors. Nature 467, 673–677 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, S. & Li, W. A color-coding amacrine cell may provide a blue-off signal in a mammalian retina. Nature Neurosci. 15, 954–956 (2012).
  Article CAS PubMed Google Scholar
• Borst, A. & Euler, T. Seeing things in motion: models, circuits, and mechanisms. Neuron 71, 974–994 (2011).
  Article CAS PubMed Google Scholar
• Briggman, K. L., Helmstaedter, M. & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188 (2011).
  Article CAS PubMed Google Scholar
• Hausselt, S. E., Euler, T., Detwiler, P. B. & Denk, W. A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol. 5, e185 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Oesch, N., Euler, T. & Taylor, W. R. Direction-selective dendritic action potentials in rabbit retina. Neuron 47, 739–750 (2005).
  Article CAS PubMed Google Scholar
• Schachter, M. J., Oesch, N., Smith, R. G. & Taylor, W. R. Dendritic spikes amplify the synaptic signal to enhance detection of motion in a simulation of the direction-selective ganglion cell. PLoS Comput. Biol. 6, e1000899 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Sivyer, B. & Williams, S. R. Direction selectivity is computed by active dendritic integration in retinal ganglion cells. Nature Neurosci. 16, 1848–1856 (2013).
  Article CAS PubMed Google Scholar
• Kim, J. S. et al. Space–time wiring specificity supports direction selectivity in the retina. Nature 509, 331–336 (2014). A demonstration in mice that OFF starburst amacrine cells tend to receive inputs from different types of bipolar cells depending on dendritic eccentricity.
  Article CAS PubMed PubMed Central Google Scholar
• Garvert, M. M. & Gollisch, T. Local and global contrast adaptation in retinal ganglion cells. Neuron 77, 915–928 (2013).
  Article CAS PubMed Google Scholar
• Bolinger, D. & Gollisch, T. Closed-loop measurements of iso-response stimuli reveal dynamic nonlinear stimulus integration in the retina. Neuron 73, 333–346 (2012).
  Article PubMed CAS Google Scholar
• Volgyi, B., Deans, M. R., Paul, D. L. & Bloomfield, S. A. Convergence and segregation of the multiple rod pathways in mammalian retina. J. Neurosci. 24, 11182–11192 (2004).
  Article PubMed PubMed Central CAS Google Scholar
• Bloomfield, S. A. & Dacheux, R. F. Rod vision: pathways and processing in the mammalian retina. Prog. Retin. Eye Res. 20, 351–384 (2001).
  Article CAS PubMed Google Scholar
• Dunn, F. A. & Rieke, F. The impact of photoreceptor noise on retinal gain controls. Curr. Opin. Neurobiol. 16, 363–370 (2006).
  Article CAS PubMed Google Scholar
• Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. Microcircuits for night vision in mouse retina. J. Neurosci. 21, 8616–8623 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Tsukamoto, Y. & Omi, N. Functional allocation of synaptic contacts in microcircuits from rods via rod bipolar to AII amacrine cells in the mouse retina. J. Comp. Neurol. 521, 3541–3555 (2013).
  Article PubMed PubMed Central Google Scholar
• Roehlich, P., Van Veen, T. & Szél, A. Two different visual pigments in one retinal cone cell. Neuron 13, 1159–1166 (1994).
  Article CAS Google Scholar
• Puller, C., Haverkamp, S. & Grünert, U. OFF midget bipolar cells in the retina of the marmoset, Callithrix jacchus, express AMPA receptors. J. Comp. Neurol. 502, 442–454 (2007).
  Article CAS PubMed Google Scholar
• Haverkamp, S. et al. The primordial, blue-cone color system of the mouse retina. J. Neurosci. 25, 5438–5445 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Neves, G. & Lagnado, L. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J. Physiol. 515, 181–202 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Pang, J. J., Gao, F. & Wu, S. M. Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF α ganglion cells in the mouse retina. J. Neurosci. 23, 6063–6073 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, I. J., Zhang, Y., Yamagata, M., Meister, M. & Sanes, J. R. Molecular identification of a retinal cell type that responds to upward motion. Nature 452, 478–482 (2008).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Ichinose, T., Fyk-Kolodziej, B. & Cohn, J. Roles of on cone bipolar cell subtypes in temporal coding in the mouse retina. J. Neurosci. 34, 8761–8771 (2014).
  Article CAS PubMed PubMed Central Google Scholar