Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-25T17:01:20.669Z Has data issue: false hasContentIssue false

Receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells

Published online by Cambridge University Press:  02 June 2009

Ralph J. Jensen
Affiliation:
Department of Biomedical Sciences, Southern College of Optometry, Memphis

Abstract

Starburst amacrine cells in the rabbit retina were labeled following an intraocular injection of the fluorescent dye, 4, 6, diamidino-2-phenylindole (DAPI). From each eye a strip of retina was removed, mounted on a platform beneath an epifluorescence microscope, and superfused with a physiological solution. The tip of a tungsten microelectrode (for extracellular recording) was visually positioned near the cell body of a DAPI-labeled starburst amacrine cell that was located in the ganglion cell layer. Light-evoked responses from the displaced starburst amacrine cells were studied in normal retinas and in retinas that had received a small electrolytic lesion near the optic disk 5–9 months beforehand. In normal retinas, a small spot of light centered over the receptive field of a displaced starburst amacrine cell in nearly all cases evoked a brief burst of spikes only at light onset. When stimulated with a large spot or an annulus of light, many cells gave a small burst of spikes at light offset. In lesioned retinas, the light responses of displaced starburst amacrine cells were recorded in areas of the retina where ganglion cells had degenerated. All cells responded with a large burst of spikes at the onset and offset of a small, centered spot of light. Large spots and annuli of light also evoked robust ON/OFF responses from these cells. The results from this study show that the receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells. This finding indicates that changes in either synaptic transmission or the membrane properties of neurons occur in the retina following degeneration of ganglion cells.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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

Berardi, N., Domenici, L., Gravina, A. & Maffei, L. (1990). Pattern ERG in rats following section of the optic nerve. Experimental Brain Research 79, 539546.CrossRefGoogle Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711725.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuroscience 6, 113.CrossRefGoogle Scholar
Hayden, S.A., Mills, J.W. & Masland, R.M. (1980). Acetylcholine synthesis by displaced amacrine cells. Science 210, 435437.CrossRefGoogle ScholarPubMed
Hollander, H., Bisti, S., Maffei, L. & Hebel, R. (1984). Electroretinographic responses and retrograde changes of retinal morphology after intracranial optic nerve section. A quantitative analysis in the cat. Experimental Brain Research 55, 483493.CrossRefGoogle ScholarPubMed
James, G.R. (1933). Degeneration of ganglion cell following axonal injury: An experimental study. Archives of Ophthalmology 9, 338343.CrossRefGoogle Scholar
Jensen, R.J. (1989). Mechanism and site of action of a dopamine D1 antagonist in the rabbit retina. Visual Neuroscience 3, 573585.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, 101112.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1993). Extracellular recordings from displaced cholinergic amacrine cells in rabbit retina. Investigative Ophthalmology and Visual Science 34, 1153.Google Scholar
Jensen, R.J. (1994). Extracellular recordings from displaced starburst amacrine cells in normal, unlesioned rabbit retinas. Investigative Ophthalmology and Visual Science 35, 2057.Google Scholar
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. Journal of Physiology 207, 623633.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510515.CrossRefGoogle ScholarPubMed
Maffei, L. & Fiorentini, A. (1981). Electroretinographic responses to alternating gratings before and after section of the optic nerve. Science 211, 953955.CrossRefGoogle Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159178.CrossRefGoogle ScholarPubMed
Masland, R.H., Mills, J.W. & Cassidy, C. (1984 a). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B 223, 121139.Google ScholarPubMed
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984 b). Acetylcholine-synthesizing amacrine cells: Identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society B 223, 79100.Google ScholarPubMed
Massey, S.C., Redburn, D.A. & Crawford, M.L.J. (1983). The effects of 2-amino-4-phosphonobutyric acid (APB) on the ERG and ganglion cell discharge of rabbit retina. Vision Research 23, 16071613.CrossRefGoogle ScholarPubMed
Miller, R.F. & Bloomfield, S.A. (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy of Science of the U.S.A. 80, 30693073.CrossRefGoogle ScholarPubMed
Miller, R.F. & Dacheux, R. (1975). Chloride-sensitive receptive field mechanisms in the isolated retina-eyecup of the rabbit. Brain Research 90, 329334.CrossRefGoogle Scholar
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931944.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Osman, K. (1986). Cytochemical identification of cholinergic amacrine cells in cat retina. Journal of Comparative Neurology 247, 497504.CrossRefGoogle ScholarPubMed
Radius, R.L. & Anderson, D.G. (1978). Retinal ganglion cell degeneration in experimental optic atrophy. American Journal of Ophthalmology 86, 673679.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1989). Starburst amacrine cells of the primate retina. Journal of Comparative Neurology 285, 1837.CrossRefGoogle ScholarPubMed
Scherer, J. & Schnitzer, J. (1991). Intraorbital transection of the rabbit optic nerve: Consequences for ganglion cells and neuroglia in the retina. Journal of Comparative Neurology 312, 175192.CrossRefGoogle ScholarPubMed
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B 223, 101119.Google ScholarPubMed
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 24942501.CrossRefGoogle ScholarPubMed
Toyoda, J., Hashimoto, H. & Ohtsu, K. (1973). Bipolar-amacrine transmission in the carp retina. Vision Research 13, 295307.CrossRefGoogle ScholarPubMed
Van Buren, J.M. (1963). Trans-synaptic retrograde degeneration in the visual system of primates. Journal of Neurology, Neurosurgery, and Psychiatry 26, 402409.Google Scholar
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B 220, 501508.Google ScholarPubMed
Vaney, D.I., Peichl, L. & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. Journal of Comparative Neurology 199, 373391.CrossRefGoogle ScholarPubMed
Voight, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 1935.CrossRefGoogle Scholar
Wässle, H., Chun, M.H. & Muller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 205, 391408.CrossRefGoogle Scholar
Werblin, F. & Dowling, J. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339355.CrossRefGoogle ScholarPubMed