Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T02:43:56.401Z Has data issue: false hasContentIssue false
  • English
  • Français

Dendritic morphology and tracer-coupling pattern of physiologically identified transient uniformity detector ganglion cells in rabbit retina

Published online by Cambridge University Press:  21 September 2010

BENJAMIN SIVYER  and
DAVID I. VANEY
BENJAMIN SIVYER*
Affiliation:
ARC Centre of Excellence in Vision Science, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
DAVID I. VANEY
Affiliation:
ARC Centre of Excellence in Vision Science, Queensland Brain Institute, The University of Queensland, Brisbane, Australia
*
*Address correspondence and reprint requests to: Benjamin Sivyer, Queensland Brain Institute, The University of Queensland, Brisbane 4072, Queensland, Australia. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Transient uniformity detectors (UDs) are a unique type of retinal ganglion cell (RGC) whose maintained firing is transiently suppressed by all types of visual stimuli. In this study, we have characterized the dendritic morphology and tracer-coupling pattern of UDs that were labeled by loose-seal electroporation of Neurobiotin following functional identification in the isolated rabbit retina. The UDs have a bistratified dendritic tree, branching near the margins of the inner plexiform layer in stratum 1 (part of the OFF sublamina) and stratum 4/5 (part of the ON sublamina). Characteristically, many of the distal dendrites in the OFF arbor do not terminate there but dive recurrently back to the ON arbor. As a consequence, the ON dendritic arbor is usually twice as large as the OFF dendritic arbor in area. The UDs sometimes show homologous tracer coupling to neighboring RGCs with the same morphology, and from this material, we estimate that the UDs have a threefold dendritic field overlap and a maximum density of ~100 cells/mm2 on the peak visual streak, accounting for ~2% of RGCs in rabbit retina. The UDs also show strong heterologous tracer coupling to a novel type of amacrine cell that costratifies with the ON arbor of the UD. Consistent with their unistratified medium-field morphology, these St4/5 amacrine cells appear to be GABAergic: their somata are immunopositive for GABA but immunonegative for glycine and glycine transporter 1. We compare the dendritic morphology of the UDs to that of other types of bistratified RGCs described in rabbit retina and note that the stratification levels and distinctive recurrent dendrites closely resemble those of the “ON bistratified diving” RGCs. This raises the possibility that there are two types of RGCs with distinctive physiological properties that have almost identical bistratified dendritic morphologies.

Keywords

Suppressed by contrastRetinal ganglion cellAmacrine cellGABAGlycine
Type
Research Articles
Information
Visual Neuroscience , Volume 27 , Issue 5-6 , November 2010 , pp. 159 - 170
Copyright
Copyright © Cambridge University Press 2010

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

Ackert, J.M., Wu, S.H., Lee, J.C., Abrams, J., Hu, E.H., Perlman, I. & Bloomfield, S.A. (2006). Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. The Journal of Neuroscience 26, 4206–4215.CrossRefGoogle ScholarPubMed
Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1983). Quantitative morphology of rabbit retinal ganglion cells. Proceedings of the Royal Society of London. Series B 217, 341–355.Google ScholarPubMed
Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.CrossRefGoogle ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 a). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. The Journal of Comparative Neurology 280, 72–96.CrossRefGoogle ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 b). Morphologies of rabbit retinal ganglion cells with complex receptive fields. The Journal of Comparative Neurology, 280, 97–121.CrossRefGoogle ScholarPubMed
Badea, T.C. & Nathans, J. (2004). Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter. The Journal of Comparative Neurology 480, 331–351.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
Bloomfield, S.A. (1994). Orientation-sensitive amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 71, 1672–1691.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. The Journal of Neuroscience 6, 1–13.CrossRefGoogle Scholar
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.CrossRefGoogle ScholarPubMed
Buhl, E.H. & Peichl, L. (1986). Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. The Journal of Comparative Neurology 253, 163–174.CrossRefGoogle Scholar
Cajal, S.R. (1893). La rétine des vertébrés. La Cellule 9, 119–257.Google Scholar
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. (1974). 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
Coombs, J., van der List, D., Wang, G.Y. & Chalupa, L.M. (2006). Morphological properties of mouse retinal ganglion cells. Neuroscience 140, 123–136.CrossRefGoogle ScholarPubMed
Dacey, D.M., Peterson, B.B., Robinson, F.R. & Gamlin, P.D. (2003). Fireworks in the primate retina: In vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27.CrossRefGoogle ScholarPubMed
DeVries, S.H. (1999). Correlated firing in rabbit retinal ganglion cells. Journal of Neurophysiology 81, 908–920.CrossRefGoogle ScholarPubMed
Dodt, H., Eder, M., Frick, A. & Zieglgansberger, W. (1999). Precisely localized LTD in the neocortex revealed by infrared-guided laser stimulation. Science 286, 110–113.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1987). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404–408.CrossRefGoogle ScholarPubMed
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. (1992). 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. (2004). Class I and class II ganglion cells of rabbit retina: Quantitative analysis of dendritic branching patterns. The Journal of Comparative Neurology 478, 347–358.CrossRefGoogle Scholar
Famiglietti, E.V. (2005). 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 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
Hamasaki, D.I., Tasaki, K. & Suzuki, H. (1979). Properties of X- and Y-cells in the rabbit retina. Japanese Journal of Physiology 29, 445–457.Google ScholarPubMed
Hampson, E.C., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. The Journal of Neuroscience 12, 4911–4922.CrossRefGoogle ScholarPubMed
He, S., Levick, W.R. & Vaney, D.I. (1998). Distinguishing direction selectivity from orientation selectivity in the rabbit retina. Visual Neuroscience 15, 439–447.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. The Journal of Neuroscience 29, 8875–8883.CrossRefGoogle Scholar
Isayama, T., Berson, D.M. & Pu, M. (2000). Theta ganglion cell type of cat retina. The Journal of Comparative Neurology 417, 32–48.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Jensen, R.J. (1991). Intracellular recording of light responses from visually identified ganglion cells in the rabbit retina. Journal of Neuroscience Methods 40, 101–112.CrossRefGoogle ScholarPubMed
Kanjhan, R. & Vaney, D.I. (2008). Semi-loose seal Neurobiotin electroporation for combined structural and functional analysis of neurons. Pflugers Archiv European Journal of Physiology 457, 561–568.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
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit’s retina. The Journal of Physiology 188, 285–307.CrossRefGoogle Scholar
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. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971–982.CrossRefGoogle ScholarPubMed
Masland, R.H. (2001). Neuronal diversity in the retina. Current Opinions in Neurobiology 11, 431–436.CrossRefGoogle ScholarPubMed
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984). Acetylcholine-synthesizing amacrine cells: Identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society of London. Series B 223, 79–100.Google ScholarPubMed
Mastronarde, D.N. (1985). Two types of cat retinal ganglion cells that are suppressed by contrast. Vision Research 25, 1195–1196.CrossRefGoogle ScholarPubMed
Nelson, R., Famiglietti, E.V., & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472–483.CrossRefGoogle ScholarPubMed
O’Brien, B.J., Isayama, T. & Berson, D.M. (1999). Light responses of morphologically identified cat ganglion cells. Investigative Ophthalmology & Visual Science 40: ARVO Abstract 815.Google Scholar
Oyster, C.W., Takahashi, E.S. & Hurst, D.C. (1981). Density, soma size, and regional distribution of rabbit retinal ganglion cells. The Journal of Neuroscience 1, 1331–1346.CrossRefGoogle ScholarPubMed
Peichl, L., Buhl, E.H. & Boycott, B.B. (1987). Alpha ganglion cells in the rabbit retina. The Journal of Comparative Neurology 263, 25–41.CrossRefGoogle ScholarPubMed
Polyak, S.L. (1941). The Retina. Chicago: University of Chicago Press.Google Scholar
Pow, D.V. & Crook, D.K. (1993). Extremely high titre polyclonal antisera against small neurotransmitter molecules: Rapid production, characterisation and use in light- and electron-microscopic immunocytochemistry. Journal of Neuroscience Methods 48, 51–63.CrossRefGoogle ScholarPubMed
Pow, D.V. & Hendrickson, A.E. (1999). Distribution of the glycine transporter glyt-1 in mammalian and nonmammalian retinae. Visual Neuroscience 16, 231–239.CrossRefGoogle ScholarPubMed
Provis, J.M. (1979). The distribution and size of ganglion cells in the retina of the pigmented rabbit: A quantitative analysis. The Journal of Comparative Neurology 185, 121–137.CrossRefGoogle ScholarPubMed
Pu, M.L. & Amthor, F.R. (1990 a). Dendritic morphologies of retinal ganglion cells projecting to the nucleus of the optic tract in the rabbit. The Journal of Comparative Neurology 302, 657–674.CrossRefGoogle Scholar
Pu, M.L. & Amthor, F.R. (1990 b). Dendritic morphologies of retinal ganglion cells projecting to the lateral geniculate nucleus in the rabbit. The Journal of Comparative Neurology 302, 675–693.CrossRefGoogle Scholar
Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P. & Masland, R.H. (2002). The diversity of ganglion cells in a mammalian retina. The Journal of Neuroscience 22, 3831–3843.CrossRefGoogle Scholar
Rodieck, R.W. (1967). Receptive fields in the cat retina: A new type. Science 157, 90–92.CrossRefGoogle ScholarPubMed
Roska, B., Molnar, A. & Werblin, F.S. (2006). Parallel processing in retinal ganglion cells: How integration of space-time patterns of excitation and inhibition form the spiking output. Journal of Neurophysiology 95, 3810–3822.CrossRefGoogle ScholarPubMed
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587.CrossRefGoogle ScholarPubMed
Roska, B. & Werblin, F. (2003). Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nature Neuroscience 6, 600–608.CrossRefGoogle ScholarPubMed
Schubert, T., Maxeiner, S., Kruger, O., Willecke, K. & Weiler, R. (2005). Connexin45 mediates gap junctional coupling of bistratified ganglion cells in the mouse retina. The Journal of Comparative Neurology 490, 29–39.CrossRefGoogle ScholarPubMed
Sivyer, B., Taylor, W.R. & Vaney, D.I. (2010). Uniformity detector retinal ganglion cells fire complex spikes and receive only light-evoked inhibition. Proceedings of the National Academy of Sciences of the United States of America 107, 5628–5633.CrossRefGoogle ScholarPubMed
Strettoi, E. & Masland, R.H. (1995). The organization of the inner nuclear layer of the rabbit retina. The Journal of Neuroscience 15, 875–888.CrossRefGoogle ScholarPubMed
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. The Journal of Neuroscience 22, 7712–7720.CrossRefGoogle ScholarPubMed
van Wyk, M., Taylor, W.R. & Vaney, D.I. (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. The Journal of Neuroscience 26, 13250–13263.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1980). A quantitative comparison between the ganglion cell populations and axonal outflows of the visual streak and periphery of the rabbit retina. The Journal of Comparative Neurology 189, 215–233.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retina Research 9, 49–100.CrossRefGoogle Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187–190.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1994 a). Territorial organization of direction-selective ganglion cells in rabbit retina. The Journal of Neuroscience 14, 6301–6316.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1994 b). Patterns of neuronal coupling in the retina. Progress in Retina Research 13, 301–355.CrossRefGoogle Scholar
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., Levick, W.R. & Thibos, L.N. (1981). Rabbit retinal ganglion cells. Receptive field classification and axonal conduction properties. Experimental Brain Research 44, 27–33.Google 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 235, 203–219.Google ScholarPubMed
Vaney, D.I., Nelson, J.C. & Pow, D.V. (1998). Neurotransmitter coupling through gap junctions in the retina. The Journal of Neuroscience 18, 10594–10602.CrossRefGoogle ScholarPubMed
Viney, T.J., Balint, K., Hillier, D., Siegert, S., Boldogkoi, Z., Enquist, L.W., Meister, M., Cepko, C.L. & Roska, B. (2007). Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Current Biology 17, 981–988.CrossRefGoogle ScholarPubMed
Völgyi, B., Chheda, S. & Bloomfield, S.A. (2009). Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. The Journal of Comparative Neurology 512, 664–687.CrossRefGoogle ScholarPubMed
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews Neuroscience 5, 747–757.CrossRefGoogle ScholarPubMed
Wässle, H., Boycott, B.B. & Illing, R.B. (1981). Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations. Proceedings of the Royal Society of London. Series B 212, 177–195.Google Scholar
Wong, R.O. (1990). Differential growth and remodelling of ganglion cell dendrites in the postnatal rabbit retina. The Journal of Comparative Neurology 294, 109–132.CrossRefGoogle ScholarPubMed
Wright, L.L., Macqueen, C.L., Elston, G.N., Young, H.M., Pow, D.V. & Vaney, D.I. (1997). The DAPI-3 amacrine cells of the rabbit retina. Visual Neuroscience 14, 473–492.CrossRefGoogle ScholarPubMed
Xin, D. & Bloomfield, S.A. (1997). Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. The Journal of Comparative Neurology 383, 512–528.3.0.CO;2-5>CrossRefGoogle ScholarPubMed