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Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina

Published online by Cambridge University Press:  06 October 2005

JIAN ZHANG ,
WEI LI ,
HIDEO HOSHI ,
STEPHEN L. MILLS  and
STEPHEN C. MASSEY
JIAN ZHANG
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Medical School at Houston, Houston Current address of Jian Zhang: Cullen Eye Institute, Baylor College of Medicine, Houston, TX 77030
WEI LI
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Medical School at Houston, Houston Current address of Wei Li: Department of Ophthalmology, Northwestern Medical School, Chicago, IL 60611
HIDEO HOSHI
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Medical School at Houston, Houston
STEPHEN L. MILLS
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Medical School at Houston, Houston
STEPHEN C. MASSEY
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Medical School at Houston, Houston
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Abstract

The correlation between cholinergic sensitivity and the level of stratification for ganglion cells was examined in the rabbit retina. As examples, we have used ON or OFF α ganglion cells and ON/OFF directionally selective (DS) ganglion cells. Nicotine, a cholinergic agonist, depolarized ON/OFF DS ganglion cells and greatly enhanced their firing rates but it had modest excitatory effects on ON or OFF α ganglion cells. As previously reported, we conclude that DS ganglion cells are the most sensitive to cholinergic drugs. Confocal imaging showed that ON/OFF DS ganglion cells ramify precisely at the level of the cholinergic amacrine cell dendrites, and co-fasciculate with the cholinergic matrix of starburst amacrine cells. However, neither ON or OFF α ganglion cells have more than a chance association with the cholinergic matrix. Z-axis reconstruction showed that OFF α ganglion cells stratify just below the cholinergic band in sublamina a while ON α ganglion cells stratify just below cholinergic b. The latter is at the same level as the terminals of calbindin bipolar cells. Thus, the calbindin bipolar cell appears to be a prime candidate to provide the bipolar cell input to ON α ganglion cells in the rabbit retina. We conclude that the precise level of stratification is correlated with the strength of cholinergic input. Alpha ganglion cells receive a weak cholinergic input and they are narrowly stratified just below the cholinergic bands.

Keywords

RetinaInner plexiform layerConfocal microscopyAlpha ganglion cellsDirectional selectivityON/OFF DS ganglion cellsCholinergic amacrine cellsCalbindin bipolar cells
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 535 - 549
Copyright
2005 Cambridge University Press

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References

REFERENCES

Ames, A.III & Nesbett, F.B. (1981). In vitro retina as an experimental model of the central nervous system. Journal of Neurochemistry 37, 867–877.Google Scholar
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, 187–90.Google Scholar
Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989a). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.Google Scholar
Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989b). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.Google Scholar
Ariel, M. & Daw, N.W. (1982a). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology (London) 324, 135–160.Google Scholar
Ariel, M. & Daw, N.W. (1982b). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161–185.Google Scholar
Baldridge, W.H. (1996). Optical recordings of the effects of cholinergic ligands on neurons in the ganglion cell layer of mammalian retina. Journal of Neuroscience 16, 5060–5072.Google Scholar
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. Journal of Physiology (London) 173, 377–407.CrossRefGoogle Scholar
Berson, D.M. (2003). Strange vision: Ganglion cells as circadian photoreceptors. Trends in Neuroscience 26, 314–320.CrossRefGoogle Scholar
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuroscience 6, 1–13.Google Scholar
Boycott, B.B. & Wässle, H. (1991). Morphological classification of bipolar cells of the primate retina. European Journal of Neuroscience 3, 1069–1088.CrossRefGoogle Scholar
Brecha, N., Johnson, D., Peichl, L., & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.CrossRefGoogle Scholar
Brown, S.P., He, S., & Masland, R.H. (2000). Receptive field microstructure and dendritic geometry of retinal ganglion cells. Neuron 27, 371–383.CrossRefGoogle Scholar
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. Journal of Physiology (London) 276, 257–276.CrossRefGoogle Scholar
Dacey, D.M., Liao, H.W., Peterson, B.B., Robinson, F.R., Smith, V.C., Pokorny, J., Yau, K.W., & Gamlin, P.D. (2005). Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433, 749–754.CrossRefGoogle Scholar
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 Scholar
DeVries, S.H. (1999). Correlated firing in rabbit retinal ganglion cells. Journal of Neurophysiology 81, 908–920.Google Scholar
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.CrossRefGoogle Scholar
DeVries, S.H. & Baylor, D.A (1997). Mosaic arrangement of ganglion cell receptive fields in rabbit retina. Journal of Neurophysiology 78, 2048–2060.Google Scholar
Dong, W., Sun, W., Zhang, Y., Chen, X., & He, S. (2004). Dendritic relationship between starburst amacrine cells and direction-selective ganglion cells in the rabbit retina. Journal of Physiology 556, 11–17.CrossRefGoogle Scholar
Famiglietti, E.V. (1992). Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. Journal of Comparative Neurology 324, 322–335.CrossRefGoogle Scholar
Famiglietti, E.V. (2004). Class I and class II ganglion cells of rabbit retina: A structural basis for X and Y (brisk) cells. Journal of Comparative Neurology 478, 323–46.CrossRefGoogle Scholar
Famiglietti, E.V., Jr. & Kolb, H. (1976). Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle Scholar
Famiglietti, E.V., Jr. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.CrossRefGoogle Scholar
Fried, S.I., Munch, T.A., & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.CrossRefGoogle Scholar
Ghosh, K.K., Bujan, S., Haverkamp, S., Feigenspan, A., & Wassle, H. (2004). Types of bipolar cells in the mouse retina. Journal of Comparative Neurology 469, 70–82.CrossRefGoogle Scholar
Hartveit, E. (1997). Functional organization of cone bipolar cells in the rat retina. Journal of Neurophysiology 77, 1716–1730.Google Scholar
Haverkamp, S., Haeseleer, F., & Hendrickson, A. (2003). A comparison of imunocytochemical markers to identify bipolar cell types in human and monkey retina. Visual Neuroscience 20, 589–600.CrossRefGoogle 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
Keyser, K.T., MacNeil, M.A., Dmitrieva, N., Wang, F., Masland, R.H., & Lindstrom, J.M. (2000). Amacrine, ganglion, and displaced amacrine cells in the rabbit retina express nicotinic acetylcholine receptors. Vis Neuroscience 17, 743–52.CrossRefGoogle Scholar
Kittila, C.A. & Massey, S.C. (1997). Pharmacology of directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 77, 675–689.Google Scholar
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E., & Masland, R.H. (2004). The population of bipolar cells in the rabbit retina. Journal of Comparative Neurology 472, 73–86.CrossRefGoogle Scholar
Marc, R.E. & Jones, B.W. (2002). Molecular phenotyping of retinal ganglion cells. Journal of Neuroscience 22, 413–427.Google Scholar
Masland, R.H. & Ames, A., III (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.Google Scholar
Masland, R.H. & Raviola, E. (2000). Confronting complexity: Strategies for understanding the microcircuitry of the retina. Annual Review of Neuroscience 23, 249–284.CrossRefGoogle Scholar
Massey, S.C. & Mills, S.L. (1996). A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. Journal of Comparative Neurology 366, 15–33.3.0.CO;2-N>CrossRefGoogle Scholar
Massey, S.C. & Mills, S.L. (1999). An antibody to calretinin stains AII amacrine cells in the rabbit retina: Double-label and confocal analyses. Journal of Comparative Neurology 411, 3–18.3.0.CO;2-1>CrossRefGoogle Scholar
Nygaard, R.W. & Frumkes, T.E. (1982). LEDs: Convenient, inexpensive sources for visual experimentation. Vision Research 22, 435–440.CrossRefGoogle Scholar
Peichl, L. (1991). Alpha ganglion cells in mammalian retinae: common properties, species differences, and some comments on other ganglion cells. Visual Neuroscience 7, 155–169.CrossRefGoogle Scholar
Peichl, L., Buhl, E.H., & Boycott, B.B. (1987). Alpha ganglion cells in the rabbit retina. Journal of Comparative Neurology 263, 25–41.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. Journal of Neuroscience 22, 3831–3843.Google Scholar
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior, and Evolution 23, 121–164.Google Scholar
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque, and baboon retinas. Journal of Comparative Neurology 321, 46–64.CrossRefGoogle Scholar
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587.CrossRefGoogle Scholar
Strang, C.E., Amthor, F.R., & Keyser, K.T. (2003). Rabbit retinal ganglion cell responses to nicotine can be mediated by beta2-containing nicotinic acetylcholine receptors. Visual Neuroscience 20, 651–662.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.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–19.CrossRefGoogle Scholar
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 2494–2501.Google Scholar
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. (2004). Type 1 nitrergic (ND1) cells of the rabbit retina: comparison with other axon-bearing amacrine cells. Journal of Comparative Neurology 474(1), 149–171.CrossRefGoogle Scholar
Vaney, D.I. & Pow, D.V. (2000). The dendritic architecture of the cholinergic plexus in the rabbit retina: Selective labeling by glycine accumulation in the presence of sarcosine. Journal of Comparative Neurology 421, 1–13.Google Scholar
Vardi, N., Massarachia, P.J., & Sterling, P. (1989). Structure of the starburst amacrine network in the cat retina and its association with alpha ganglion cells. Journal of Comparative Neurology 288, 601–611.CrossRefGoogle Scholar
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.CrossRefGoogle Scholar
Weng, S., Sun, W., & He, S. (2005). Identification of ON–OFF direction-selective ganglion cells in the mouse retina. Journal of Physiology 562, 915–923.CrossRefGoogle Scholar
Yamada, E.S., Bordt, A.S., & Marshak, D.W. (2005). Wide-field ganglion cells in macaque retinas. Visual Neuroscience 22, 379–389.CrossRefGoogle Scholar
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. Journal of Comparative Neurology 310, 139–153.CrossRefGoogle Scholar
Zheng, J.J., Lee, S., & Zhou, Z.J. (2004). A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44, 851–864.CrossRefGoogle Scholar