Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-23T20:39:37.872Z Has data issue: false hasContentIssue false
  • English
  • Français

Synaptic inputs from identified bipolar and amacrine cells to a sparsely branched ganglion cell in rabbit retina

Published online by Cambridge University Press:  01 April 2019

Andrea S. Bordt ,
Diego Perez ,
Luke Tseng ,
Weiley Sunny Liu ,
Jay Neitz ,
Sara S. Patterson ,
Edward V. Famiglietti  and
David W. Marshak
Andrea S. Bordt
Affiliation:
Department of Neurobiology and Anatomy, McGovern Medical School, Houston, Texas 77030, USA
Diego Perez
Affiliation:
Department of Neurobiology and Anatomy, McGovern Medical School, Houston, Texas 77030, USA
Luke Tseng
Affiliation:
Department of Neurobiology and Anatomy, McGovern Medical School, Houston, Texas 77030, USA
Weiley Sunny Liu
Affiliation:
Department of Neurobiology and Anatomy, McGovern Medical School, Houston, Texas 77030, USA
Jay Neitz
Affiliation:
Department of Ophthalmology, University of Washington, Seattle, Washington 98109, USA
Sara S. Patterson
Affiliation:
Department of Ophthalmology, University of Washington, Seattle, Washington 98109, USA
Edward V. Famiglietti
Affiliation:
Department of Molecular Pharmacology, Physiology, and Biotechnology, Brown University, and Division of Ophthalmology, Rhode Island Hospital, Providence, Rhode Island 02903, USA
David W. Marshak*
Affiliation:
Department of Neurobiology and Anatomy, McGovern Medical School, Houston, Texas 77030, USA
*
*Address correspondence to: David W. Marshak, Email: david.w.marshak@uth.tmc.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

There are more than 30 distinct types of mammalian retinal ganglion cells, each sensitive to different features of the visual environment. In rabbit retina, they can be grouped into four classes according to their morphology and stratification of their dendrites in the inner plexiform layer (IPL). The goal of this study was to describe the synaptic inputs to one type of Class IV ganglion cell, the third member of the sparsely branched Class IV cells (SB3). One cell of this type was partially reconstructed in a retinal connectome developed using automated transmission electron microscopy (ATEM). It had slender, relatively straight dendrites that ramify in the sublamina a of the IPL. The dendrites of the SB3 cell were always postsynaptic in the IPL, supporting its identity as a ganglion cell. It received 29% of its input from bipolar cells, a value in the middle of the range for rabbit retinal ganglion cells studied previously. The SB3 cell typically received only one synapse per bipolar cell from multiple types of presumed OFF bipolar cells; reciprocal synapses from amacrine cells at the dyad synapses were infrequent. In a few instances, the bipolar cells presynaptic to the SB3 ganglion cell also provided input to an amacrine cell presynaptic to the ganglion cell. There was apparently no crossover inhibition from narrow-field ON amacrine cells. Most of the amacrine cell inputs were from axons and dendrites of GABAergic amacrine cells, likely providing inhibitory input from outside the classical receptive field.

Keywords

Neural circuitsInterneuronProjection neuronSynapseElectron microscopy
Type
Research Article
Information
Visual Neuroscience , Volume 36 , 2019 , E004
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, J.R., Jones, B.W., Watt, C.B., Shaw, M.V., Yang, J.H., Demill, D., Lauritzen, J.S., Lin, Y., Rapp, K.D., Mastronarde, D., Koshevoy, P., Grimm, B., Tasdizen, T., Whitaker, R. & Marc, R.E. (2011a). Exploring the retinal connectome. Molecular Vision 17, 355–379.Google Scholar
Anderson, J.R., Jones, B.W., Yang, J.H., Shaw, M.V., Watt, C.B., Koshevoy, P., Spaltenstein, J., Jurrus, E., Kannan, U.V., Whitaker, R.T., Mastronarde, D., Tasdizen, T. & Marc, R.E. (2009). A computational framework for ultrastructural mapping of neural circuitry. PLoS Biology 7, e1000074.CrossRefGoogle ScholarPubMed
Anderson, J.R., Mohammed, S., Grimm, B., Jones, B.W., Koshevoy, P., Tasdizen, T., Whitaker, R. & Marc, R.E. (2011b). The Viking viewer for connectomics: Scalable multi-user annotation and summarization of large volume data sets. Journal of Microscopy 241, 13–28.CrossRefGoogle Scholar
Baccus, S.A. (2007). Timing and computation in inner retinal circuitry. Annual Review of Physiology 69, 271–290.CrossRefGoogle ScholarPubMed
Baden, T., Berens, P., Franke, K., Roman Roson, M., Bethge, M. & Euler, T. (2016). The functional diversity of retinal ganglion cells in the mouse. Nature 529, 345–350.CrossRefGoogle ScholarPubMed
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. The Journal of Physiology 173, 377–407.CrossRefGoogle ScholarPubMed
Beaudoin, D.L., Kupershtok, M. & Demb, J.B. (2017). Selective synaptic connections in the retinal pathway for night vision. The Journal of Comparative Neurology.Google ScholarPubMed
Beaudoin, D.L., Kupershtok, M. & Demb, J.B. (2019). Selective synaptic connections in the retinal pathway for night vision. Journal of Comparative Neurology 527, 117–132.CrossRefGoogle ScholarPubMed
Berson, D.M. (2003). Strange vision: Ganglion cells as circadian photoreceptors. Trends in Neurosciences 26, 314–320.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1991). Two types of orientation-sensitive responses of amacrine cells in the mammalian retina. Nature 350, 347–350.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1994). Orientation-sensitive amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 71, 1672–1691.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat’s retina. The Journal of Physiology 240, 397–419.CrossRefGoogle ScholarPubMed
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. The Journal of Physiology 276, 257–276.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974a). Brisk and sluggish concentrically organized ganglion cells in the cat’s retina. The Journal of Physiology 240, 421–456.CrossRefGoogle Scholar
Cleland, B.G. & Levick, W.R. (1974b). Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification. The Journal of Physiology 240, 457–492.CrossRefGoogle Scholar
Dacheux, R.F., Chimento, M.F. & Amthor, F.R. (2003). Synaptic input to the on-off directionally selective ganglion cell in the rabbit retina. The Journal of Comparative Neurology 456, 267–278.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1981). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1563.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1985). Starburst amacrine cells: Morphological constancy and systematic variation in the anisotropic field of rabbit retinal neurons. Journal of Neuroscience 5, 562–577.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1987). Morphological classification of ganglion cells in rabbit retina. Society for Neuroscience Abstract 13, 380.Google Scholar
Famiglietti, E.V. (1990). A distinct type of displaced ganglion cell in a mammalian retina. Brain Research 535, 169–173.CrossRefGoogle Scholar
Famiglietti, E.V. (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. The Journal of Comparative Neurology 309, 40–70.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992a). Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. The Journal of Comparative Neurology 324, 322–335.CrossRefGoogle Scholar
Famiglietti, E.V. (1992b). New metrics for analysis of dendritic branching patterns demonstrating similarities and differences in ON and ON-OFF directionally selective retinal ganglion cells. The Journal of Comparative Neurology 324, 295–321.CrossRefGoogle Scholar
Famiglietti, E.V. (1992c). Polyaxonal amacrine cells of rabbit retina: Morphology and stratification of PA1 cells. The Journal of Comparative Neurology 316, 391–405.CrossRefGoogle Scholar
Famiglietti, E.V. (1992d). Polyaxonal amacrine cells of rabbit retina: PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation. The Journal of Comparative Neurology 316, 422–446.CrossRefGoogle Scholar
Famiglietti, E.V. (1992e). Polyaxonal amacrine cells of rabbit retina: Size and distribution of PA1 cells. The Journal of Comparative Neurology 316, 406–421.CrossRefGoogle Scholar
Famiglietti, E.V. (2002). A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells. Visual Neuroscience 19, 145–162.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (2004). Class I and class II ganglion cells of rabbit retina: A structural basis for X and Y (brisk) cells. The Journal of Comparative Neurology 478, 323–346.CrossRefGoogle Scholar
Famiglietti, E.V. (2005a). “Small-tufted” ganglion cells and two visual systems for the detection of object motion in rabbit retina. Visual Neuroscience 22, 509–534.CrossRefGoogle Scholar
Famiglietti, E.V. (2005b). Synaptic organization of complex ganglion cells in rabbit retina: Type and arrangement of inputs to directionally selective and local-edge-detector cells. The Journal of Comparative Neurology 484, 357–391.CrossRefGoogle Scholar
Famiglietti, E.V. (2008). Wide-field cone bipolar cells and the blue-ON pathway to color-coded ganglion cells in rabbit retina. Visual Neuroscience 25, 53–66.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (2009). Bistratified ganglion cells of rabbit retina: Neural architecture for contrast-independent visual responses. Visual Neuroscience 26, 195–213.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (2016). Neural architecture of the “transient” ON directionally selective (class IIb1) ganglion cells in rabbit retina, partly co-stratified with starburst amacrine cells. Visual Neuroscience 33, E004.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic cirucitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle ScholarPubMed
Franke, K., Berens, P., Schubert, T., Bethge, M., Euler, T. & Baden, T. (2017). Inhibition decorrelates visual feature representations in the inner retina. Nature 542, 439–444.CrossRefGoogle ScholarPubMed
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 2303–2320.CrossRefGoogle ScholarPubMed
Grimes, W.N., Zhang, J., Graydon, C.W., Kachar, B. & Diamond, J.S. (2010). Retinal parallel processors: More than 100 independent microcircuits operate within a single interneuron. Neuron 65, 873–885.CrossRefGoogle ScholarPubMed
Hoshi, H., Liu, W.L., Massey, S.C. & Mills, S.L. (2009). ON inputs to the OFF layer: Bipolar cells that break the stratification rules of the retina. Journal of Neuroscience 29, 8875–8883.CrossRefGoogle ScholarPubMed
Hughes, S., Jagannath, A., Rodgers, J., Hankins, M.W., Peirson, S.N. & Foster, R.G. (2016). Signalling by melanopsin (OPN4) expressing photosensitive retinal ganglion cells. Eye 30, 247–254.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1991). Involvement of glycinergic neurons in the diminished surround activity of ganglion cells in the dark-adapted rabbit retina. Visual Neuroscience 6, 43–53.CrossRefGoogle ScholarPubMed
Jones, B.W., Kondo, M., Terasaki, H., Watt, C.B., Rapp, K., Anderson, J., Lin, Y., Shaw, M.V., Yang, J.H. & Marc, R.E. (2011). Retinal remodeling in the Tg P347L rabbit, a large-eye model of retinal degeneration. The Journal of Comparative Neurology 519, 2713–2733.CrossRefGoogle Scholar
Kim, T., Soto, F. & Kerschensteiner, D. (2015). An excitatory amacrine cell detects object motion and provides feature-selective input to ganglion cells in the mouse retina. eLife 4, e08025.CrossRefGoogle ScholarPubMed
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. The Journal of Comparative Neurology 318, 147–187.CrossRefGoogle ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
Lauritzen, J.S., Anderson, J.R., Jones, B.W., Watt, C.B., Mohammed, S., Hoang, J.V. & Marc, R.E. (2013). ON cone bipolar cell axonal synapses in the OFF inner plexiform layer of the rabbit retina. The Journal of Comparative Neurology 521, 977–1000.CrossRefGoogle ScholarPubMed
Lauritzen, J.S., Sigulinsky, C.L., Anderson, J.R., Kalloniatis, M., Nelson, N.T., Emrich, D.P., Rapp, C., McCarthy, N., Kerzner, E., Meyer, M., Jones, B.W. & Marc, R.E. (2016). Rod-cone crossover connectome of mammalian bipolar cells. The Journal of Comparative Neurology 527, 87–116.CrossRefGoogle ScholarPubMed
Lee, S., Chen, L., Chen, M., Ye, M., Seal, R.P. & Zhou, Z.J. (2014). An unconventional glutamatergic circuit in the retina formed by vGluT3 amacrine cells. Neuron 84, 708–715.CrossRefGoogle ScholarPubMed
Lee, S., Zhang, Y., Chen, M. & Zhou, Z.J. (2016). Segregated glycine-glutamate Co-transmission from vGluT3 amacrine cells to contrast-suppressed and contrast-enhanced retinal circuits. Neuron 90, 27–34.CrossRefGoogle ScholarPubMed
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina. The Journal of Physiology 188, 285–307.CrossRefGoogle ScholarPubMed
Li, W., Chen, S. & DeVries, S.H. (2010). A fast rod photoreceptor signaling pathway in the mammalian retina. Nature Neuroscience 13, 414–416.CrossRefGoogle ScholarPubMed
Li, W., Keung, J.W. & Massey, S.C. (2004). Direct synaptic connections between rods and OFF cone bipolar cells in the rabbit retina. The Journal of Comparative Neurology 474, 1–12.CrossRefGoogle ScholarPubMed
Liu, P.C. & Chiao, C.C. (2007). Morphologic identification of the OFF-type blue cone bipolar cell in the rabbit retina. Investigative Ophthalmology & Visual Science 48, 3388–3395.CrossRefGoogle ScholarPubMed
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photofilled with golgi-stained cells in the rabbit retina and comparison with other mammalian species. The Journal of Comparative Neurology 413, 305–326.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (2004). The population of bipolar cells in the rabbit retina. The Journal of Comparative Neurology 472, 73–86.CrossRefGoogle ScholarPubMed
Marc, R.E., Anderson, J.R., Jones, B.W., Sigulinsky, C.L. & Lauritzen, J.S. (2014). The AII amacrine cell connectome: A dense network hub. Frontiers in Neural Circuits 8, 104.CrossRefGoogle ScholarPubMed
Marc, R.E., Jones, B.W., Watt, C.B., Anderson, J.R., Sigulinsky, C. & Lauritzen, S. (2013). Retinal connectomics: Towards complete, accurate networks. Progress in Retinal and Eye Research 37, 141–162.CrossRefGoogle ScholarPubMed
Marshak, D.W. (2016). A tale of two neurotransmitters. Visual Neuroscience 33, E017.CrossRefGoogle ScholarPubMed
McGillem, G.S. & Dacheux, R.F. (2001). Rabbit cone bipolar cells: Correlation of their morphologies with whole-cell recordings. Visual Neuroscience 18, 675–685.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. Journal of Neuroscience 6, 907–918.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1992). Morphology of bipolar cells labeled by DAPI in the rabbit retina. The Journal of Comparative Neurology 321, 133–149.CrossRefGoogle ScholarPubMed
Mills, S.L., Tian, L.M., Hoshi, H., Whitaker, C.M. & Massey, S.C. (2014). Three distinct blue-green color pathways in a mammalian retina. Journal of Neuroscience 34, 1760–1768.CrossRefGoogle Scholar
Murphy-Baum, B.L. & Taylor, W.R. (2015). The synaptic and morphological basis of orientation selectivity in a polyaxonal amacrine cell of the rabbit retina. Journal of Neuroscience 35, 13336–13350.CrossRefGoogle Scholar
Pu, M.L. & Amthor, F.R. (1990). Dendritic morphologies of retinal ganglion cells projecting to the lateral geniculate nucleus in the rabbit. The Journal of Comparative Neurology 302, 675–693.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Watanabe, M. (1993). Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. The Journal of Comparative Neurology 338, 289–303.CrossRefGoogle ScholarPubMed
Sanes, J.R. & Masland, R.H. (2015). The types of retinal ganglion cells: Current status and implications for neuronal classification. Annual Review of Neuroscience 38, 221–246.CrossRefGoogle ScholarPubMed
Sivyer, B. & Vaney, D.I. (2010). Dendritic morphology and tracer-coupling pattern of physiologically identified transient uniformity detector ganglion cells in rabbit retina. Visual Neuroscience 27, 159–170.CrossRefGoogle ScholarPubMed
Soto, F., Bleckert, A., Lewis, R., Kang, Y., Kerschensteiner, D., Craig, A.M. & Wong, R.O. (2011). Coordinated increase in inhibitory and excitatory synapses onto retinal ganglion cells during development. Neural Development 6, 31.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987). X-cells in the cat retina: Relationships between the morphology and physiology of a class of cat retinal ganglion cells. Journal of Neurophysiology 58, 940–964.CrossRefGoogle ScholarPubMed
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 37, 722–748.CrossRefGoogle ScholarPubMed
Strettoi, E. & Masland, R.H. (1995). The organization of the inner nuclear layer of the rabbit retina. Journal of Neuroscience 15, 875–888.CrossRefGoogle ScholarPubMed
Tien, N.W., Kim, T. & Kerschensteiner, D. (2016). Target-specific glycinergic transmission from VGluT3-expressing amacrine cells shapes suppressive contrast responses in the retina. Cell Reports 15, 1369–1375.CrossRefGoogle ScholarPubMed
Vaney, D.I. (2004). Type 1 nitrergic (ND1) cells of the rabbit retina: Comparison with other axon-bearing amacrine cells. The Journal of Comparative Neurology 474, 149–171.CrossRefGoogle ScholarPubMed
Vaney, D.I., Peichl, L. & Boycott, B.B. (1988). Neurofibrillar long-range amacrine cells in mammalian retinae. Proceedings of the Royal Society of London Series B, Biological Sciences 235, 203–219.Google ScholarPubMed
Volgyi, B., Xin, D., Amarillo, Y. & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. The Journal of Comparative Neurology 440, 109–125.CrossRefGoogle ScholarPubMed
Wassle, H., Puller, C., Muller, F. & Haverkamp, S. (2009). Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. Journal of Neuroscience 29, 106–117.CrossRefGoogle ScholarPubMed
Watanabe, M., Fukuda, Y., Hsiao, C.F., & Ito, H. (1985). Electron microscopic analysis of amacrine and bipolar cell inputs on Y-, X-, and W-cells in the cat retina. Brain Research 358, 229–40.CrossRefGoogle Scholar
Werblin, F.S. (2011). The retinal hypercircuit: A repeating synaptic interactive motif underlying visual function. The Journal of Physiology 589, 3691–3702.CrossRefGoogle ScholarPubMed
West, R.W. & Dowling, J.E. (1972). Synapses onto different morphological types of retinal ganglion cells. Science 178, 510–512.CrossRefGoogle ScholarPubMed
Yamada, E.S., Bordt, A.S. & Marshak, D.W. (2005). Wide-field ganglion cells in macaque retinas. Visual Neuroscience 22, 383–393.CrossRefGoogle ScholarPubMed