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The type 1 polyaxonal amacrine cells of the rabbit retina: A tracer-coupling study

Published online by Cambridge University Press:  23 June 2004

LAYNE L. WRIGHT  and
DAVID I. VANEY
LAYNE L. WRIGHT
Affiliation:
Vision, Touch & Hearing Research Centre, School of Biomedical Sciences, Queensland Brain Institute, The University of Queensland, Brisbane 4072, Queensland, Australia
DAVID I. VANEY
Affiliation:
Vision, Touch & Hearing Research Centre, School of Biomedical Sciences, Queensland Brain Institute, The University of Queensland, Brisbane 4072, Queensland, Australia
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Abstract

The type 1 polyaxonal (PA1) cell is a distinct type of axon-bearing amacrine cell whose soma commonly occupies an interstitial position in the inner plexiform layer; the proximal branches of the sparse dendritic tree produce 1–4 axon-like processes, which form an extensive axonal arbor that is concentric with the smaller dendritic tree (Dacey, 1989; Famiglietti, 1992a,b). In this study, intracellular injections of Neurobiotin have revealed the complete dendritic and axonal morphology of the PA1 cells in the rabbit retina, as well as labeling the local array of PA1 cells through homologous tracer coupling. The dendritic-field area of the PA1 cells increased from a minimum of 0.15 mm2 (0.44-mm equivalent diameter) on the visual streak to a maximum of 0.67 mm2 (0.92-mm diameter) in the far periphery; the axonal-field area also showed a 3-fold variation across the retina, ranging from 3.1 mm2 (2.0-mm diameter) to 10.2 mm2 (3.6-mm diameter). The increase in dendritic- and axonal-field size was accompanied by a reduction in cell density, from 60 cells/mm2 in the visual streak to 20 cells/mm2 in the far periphery, so that the PA1 cells showed a 12 times overlap of their dendritic fields across the retina and a 200–300 times overlap of their axonal fields. Consequently, the axonal plexus was much denser than the dendritic plexus, with each square millimeter of retina containing ∼100 mm of dendrites and ∼1000 mm of axonal processes. The strong homologous tracer coupling revealed that ∼45% of the PA1 somata were located in the inner nuclear layer, ∼50% in the inner plexiform layer, and ∼5% in the ganglion cell layer. In addition, the Neurobiotin-injected PA1 cells sometimes showed clear heterologous tracer coupling to a regular array of small ganglion cells, which were present at half the density of the PA1 cells. The PA1 cells were also shown to contain elevated levels of γ-aminobutyric acid (GABA), like other axon-bearing amacrine cells.

Keywords

Gap junctionNeurobiotinGABA
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 2 , March 2004 , pp. 145 - 155
Copyright
2004 Cambridge University Press

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References

REFERENCES

Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.CrossRefGoogle Scholar
Bloomfield, S.A., Xin, D., & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565–576.CrossRefGoogle Scholar
Brecha, N.C., Oyster, C.W., & Takahashi, E.S. (1984). Identification and characterization of tyrosine hydroxylase immunoreactive amacrine cells. Investigative Ophthalmology and Visual Science 25, 66–70.Google Scholar
Cook, P.B. & Werblin, F.S. (1994). Spike initiation and propagation in wide field transient amacrine cells of the salamander retina. Journal of Neuroscience 14, 3852–3861.Google Scholar
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque monkey retina. Journal of Comparative Neurology 284, 275–293.CrossRefGoogle Scholar
Dacey, D.M. (1990). The dopaminergic amacrine cell. Journal of Comparative Neurology 301, 461–489.CrossRefGoogle Scholar
Ehinger, B. (1966). Adrenergic retinal neurons. Zeitschrift für Zellforschung 71, 146–152.CrossRefGoogle Scholar
Famiglietti, E.V. (1989). Structural organization and development of dorsally-directed (vertical) asymmetrical amacrine cells in rabbit retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 169–180. Berlin: Springer.CrossRef
Famiglietti, E.V. (1992a). Polyaxonal amacrine cells of rabbit retina: Morphology and stratification of PA1 cells. Journal of Comparative Neurology 316, 391–405.Google Scholar
Famiglietti, E.V. (1992b). Polyaxonal amacrine cells of rabbit retina: Size and distribution of PA1 cells. Journal of Comparative Neurology 316, 406–421.Google Scholar
Famiglietti, E.V. (1992c). Polyaxonal amacrine cells of rabbit retina: PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation. Journal of Comparative Neurology 316, 422–446.Google Scholar
Goddard, J.C., Behrens, U.D., Wagner, H.J., & Djamgoz, M.B. (1991). Biocytin: Intracellular staining, dye-coupling and immunocytochemistry in carp retina. Neuroreport 2, 755–758.CrossRefGoogle Scholar
Häggendal, J. & Malmfors, T. (1965). Identification and cellular localization of the catecholamines in the retina and choroid of the rabbit. Acta Physiologica Scandinavica 64, 58–66.CrossRefGoogle Scholar
Hampson, E.C.G.M., Vaney, D.I., & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 4911–4922.Google Scholar
Hu, E.H. & Bloomfield, S.A. (2003). Gap junctional coupling underlies the short-latency spike synchrony of retinal α ganglion cells. Journal of Neuroscience 23, 6768–6777.Google Scholar
Hughes, A. & Vaney, D.I. (1981). Contact lenses change the projection of visual field onto rabbit peripheral retina Vision Research 21, 955–956.Google Scholar
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina. 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. Journal of Comparative Neurology 413, 305–326.3.0.CO;2-E>CrossRefGoogle Scholar
Marc, R.E. (2003). Retinal neurotransmitters. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 304–319. Cambridge, Mass: MIT Press.
Mastronarde, D.N. (1983). Interactions between ganglion cells in cat retina. Journal of Neurophysiology 49, 350–365.CrossRefGoogle Scholar
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734–737.CrossRefGoogle Scholar
Negishi, K. & Teranishi, T. (1990). Close tip-to-tip contacts between dendrites of transient amacrine cells in carp retina. Neuroscience Letters 115, 1–6.Google Scholar
Pow, D.V., Wright, L.L., & Vaney, D.I. (1995). The immunocytochemical detection of amino-acid neurotransmitters in paraformaldehyde-fixed tissues. Journal of Neuroscience Methods 56, 115–123.CrossRefGoogle Scholar
Stafford, D.K. & Dacey, D.M. (1997). Physiology of the A1 amacrine: A spiking, axon-bearing interneuron of the macaque monkey retina. Visual Neuroscience 14, 507–522.CrossRefGoogle Scholar
Strettoi, E. & Masland, R.H. (1996). The number of unidentified amacrine cells in the mammalian retina. Proceedings of the National Academy of Sciences of the U.S.A. 93, 14906–14911.CrossRefGoogle Scholar
Tauchi, M., Madigan, N.K., & Masland, R.H. (1990). Shapes and distributions of the catecholamine-accumulating neurons in the rabbit retina. Journal of Comparative Neurology 293, 178–189.CrossRefGoogle Scholar
Trexler, E.B., Li, W., Mills, S.L., & Massey, S.C. (2001). Coupling from AII amacrine cells to ON cone bipolar cells is bidirectional. Journal of Comparative Neurology 437, 408–422.CrossRefGoogle Scholar
Umino, O., Maehara, M., Hidaka, S., Kita, S., & Hashimoto, Y. (1994). The network properties of bipolar-bipolar cell coupling in the retina of teleost fishes. Visual Neuroscience 11, 533–548.CrossRefGoogle Scholar
van Wyk, M., Taylor, W.R., & Vaney, D.I. (2003). Local-edge-detectors in the rabbit retina: Dendritic morphology, tracer-coupling pattern and receptive-field properties of small-field ganglion cells. Society for Neuroscience 2003 Abstract Viewer, Program No. 698. 15.
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B (London) 220, 501–508.CrossRefGoogle Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal 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 Scholar
Vaney, D.I. (1992). Photochromic intensification of diaminobenzidine reaction product in the presence of tetrazolium salts: Applications for intracellular labelling and immunohistochemistry. Journal of Neuroscience Methods 44, 217–223.CrossRefGoogle Scholar
Vaney, D.I. (1994a). Patterns of neuronal coupling in the retina. Progress in Retinal and Eye Research 13, 301–355.Google Scholar
Vaney, D.I. (1994b). Territorial organization of direction-selective ganglion cells in rabbit retina. Journal of Neuroscience 14, 6301–6316.Google Scholar
Vaney, D.I. (1996). Cell coupling in the retina. In Gap Junctions in the Nervous System, ed. Spray, D.C. & Dermietzel, R., pp. 79–102. Austin, Texas: R.G. Landes.CrossRef
Vaney, D.I. (2003). Retinal amacrine cells. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 395–409. Cambridge, Massachusetts: MIT Press.
Vaney, D.I. (2004). The type 1 nitrergic (ND1) cells of the rabbit retina: Comparison with other axon-bearing amacrine cells. Journal of Comparative Neurology (in press).CrossRefGoogle Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474, 380–385.CrossRefGoogle Scholar
Vaney, D.I., Peichl, L., & Boycott, B.B. (1988). Neurofibrillar long-range amacrine cells in mammalian retinae. Proceedings of the Royal Society B (London) 235, 203–219.CrossRefGoogle Scholar
Veruki, M.L. & Hartveit, E. (2002). Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. Journal of Neuroscience 22, 10558–10566.Google Scholar
Völgyi, B. & Bloomfield, S.A. (2002). Axonal neurofilament-H immunolabeling in the rabbit retina. Journal of Comparative Neurology 453, 269–279.CrossRefGoogle Scholar
Völgyi, B., Xin, D., Amarillo, Y., & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. Journal of Comparative Neurology 440, 109–125.CrossRefGoogle Scholar
Wright, L.L. (1998). Amacrine cells of the rabbit retina. PhD Thesis, University of Queensland, Brisbane.
Wright, L.L. & Vaney, D.I. (1999). The fountain amacrine cells of the rabbit retina. Visual Neuroscience 16, 1145–1156.CrossRefGoogle Scholar
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 Scholar
Xin, D. & Bloomfield, S.A. (1997). Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. Journal of Comparative Neurology 383, 512–528.3.0.CO;2-5>CrossRefGoogle Scholar
Xin, D. & Bloomfield, S.A. (1999). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. Journal of Comparative Neurology 405, 75–87.3.0.CO;2-D>CrossRefGoogle Scholar