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Cellular positioning and dendritic field size of cholinergic amacrine cells are impervious to early ablation of neighboring cells in the mouse retina

Published online by Cambridge University Press:  03 May 2004

REZA FARAJIAN ,
MARY A. RAVEN ,
KAREN CUSATO  and
BENJAMIN E. REESE
REZA FARAJIAN
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
MARY A. RAVEN
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
KAREN CUSATO
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
BENJAMIN E. REESE
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
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Abstract

We have examined the role of neighbor relationships between cholinergic amacrine cells upon their positioning and dendritic field size by producing partial ablations of this population of cells during early development. We first determined the effectiveness of l-glutamate as an excitotoxin for ablating cholinergic amacrine cells in the developing mouse retina. Subcutaneous injections (4 mg/g) made on P-3 and thereafter were found to produce a near-complete elimination, while injections at P-2 were ineffective. Lower doses on P-3 produced only partial reductions, and were subsequently used to examine the effect of partial ablation upon mosaic organization and dendritic growth of the remaining cells. Four different Voronoi-based measures of mosaic geometry were examined in l-glutamate-treated and normal (saline-treated) retinas. Partial depletions of around 40% produced cholinergic mosaics that, when scaled for density, approximated the mosaic geometry of the normal retina. Separate comparisons simulating a 40% random deletion of the normal retina produced mosaics that were no different from those experimentally depleted retinas. Consequently, no evidence was found for positional regulation in the absence of normal neighbor relationships. Single cells in the ganglion cell layer were intracellularly filled with Lucifer Yellow to examine the morphology and dendritic field extent following partial ablation of the cholinergic amacrine cells. No discernable effect was found on their starburst morphology, and total dendritic field area, number of primary dendrites, and branch frequency were not significantly different. Cholinergic amacrine cells normally increase their dendritic field area after P-3 in excess of retinal expansion; despite this, the present results show that this growth is not controlled by the density of neighboring processes.

Keywords

ExcitotoxicityGlutamatePlasticityMorphologyRegularityStratificationCoverage factor
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 1 , January 2004 , pp. 13 - 22
Copyright
2004 Cambridge University Press

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References

REFERENCES

Amthor, F.R. & Oyster, C.W. (1995). Spatial organization of retinal information about the direction of image motion. Proceedings of the National Academy of Sciences of the U.S.A. 92, 4002–4005.CrossRefGoogle Scholar
Ault, S.J., Thompson, K.G., Zhou, Y., & Leventhal, A.G. (1993). Selective depletion of beta cells affects the development of alpha cells in cat retina. Visual Neuroscience 10, 237–245.CrossRefGoogle Scholar
Badea, T.C., Wang, Y., & Nathans, J. (2003). A noninvasive genetic/pharmacologic strategy for visualizing cell morphology and clonal relationships in the mouse. Journal of Neuroscience 23, 2314–2322.Google Scholar
Brandon, C. (1987). Cholinergic neruons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.CrossRefGoogle Scholar
Chun, M.-H., Park, S.-J., Kim, I.-B., Moon, H.-I., Kang, W.-S., Oh, S.-J., & Chung, J.-W. (2001). Excessive L-glutamate induces selective neuronal death in the developing rat retina. Association for Research in Vision and Ophthalmology Abstracts 42, 4013.Google Scholar
Cook, J.E. (1996). Spatial properties of retinal mosaics: An empirical evaluation of some existing measures. Visual Neuroscience 13, 15–30.CrossRefGoogle Scholar
Deplano, S., Gargini, C., & Bisti, S. (1999). Electrical activity regulates dendritic reorganization in ganglion cells after neonatal retinal lesion in the cat. Journal of Comparative Neurology 405, 262–270.3.0.CO;2-4>CrossRefGoogle Scholar
Dhingra, N.K., Ramamohan, Y., & Raju, T.R. (1997). Developmental expression of synaptophysin, synapsin I and syntaxin in the rat retina. Developmental Brain Research 102, 267–273.CrossRefGoogle Scholar
Eglen, S.J., van Ooyen, A., & Willshaw, D.J. (2000). Lateral cell movement driven by dendritic interactions is sufficient to form retinal mosaics. Network: Computation in Neural Systems 11, 103–118.CrossRefGoogle Scholar
Eysel, U.T., Peichl, L., & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and sensitive period. Journal of Comparative Neurology 242, 134–145.CrossRefGoogle Scholar
Famiglietti, E.V. (1983). “Starburst” amacrine cells and cholinergic neurons: Mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138–144.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. Journal of Comparative Neurology 309, 40–70.CrossRefGoogle Scholar
Fischer, A.J., Pickett Seltner, R.L., Poon, J., & Stell, W.K. (1998). Immunocytochemical characterization of quisqualic acid- and N-methyl-D-aspartate-induced excitotoxicity in the retina of chicks. Journal of Comparative Neurology 393, 1–15.Google Scholar
Galli-Resta, L. (2000). Local, possibly contact-mediated signalling restricted to homotypic neurons controls the regular spacing of cells within the cholinergic arrays in the developing rodent retina. Development 127, 1509–1516.Google Scholar
Galli-Resta, L. (2002). Putting neurons in the right places: Local interactions in the genesis of retinal architecture. Trends in Neurosciences 25, 638–643.CrossRefGoogle Scholar
Galli-Resta, L., Resta, G., Tan, S.-S., & Reese, B.E. (1997). Mosaics of islet-1 expressing amacrine cells assembled by short range cellular interactions. Journal of Neuroscience 17, 7831–7838.Google Scholar
Galli-Resta, L., Novelli, E., Volpini, M., & Strettoi, E. (2000). The spatial organization of cholinergic mosaics in the adult mouse retina. European Journal of Neuroscience 12, 3819–3822.CrossRefGoogle Scholar
Galli-Resta, L., Novelli, E., & Viegi, A. (2002). Dynamic microtubule-dependent interactions position homotypic neurones in regular monolayered arrays during retinal development. Development 129, 3803–3814.Google Scholar
Grueber, W.B., Ye, B., Moore, A.W., Jan, L.Y., & Jan, Y.N. (2003). Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Current Biology 13, 618–626.CrossRefGoogle Scholar
He, S., Weiler, R., & Vaney, D.I. (2000). Endogenous dopaminergic regulation of horizontal cell coupling in the mammalian retina. Journal of Comparative Neurology 418, 33–40.3.0.CO;2-J>CrossRefGoogle Scholar
Honjo, M., Tanihara, H., Suzuki, S., Tanaka, T., Honda, Y., & Takeichi, M. (2000). Differential expression of cadherin adhesion receptors in neural retina of the postnatal mouse. Investigative Ophthalmology and Visual Science 41, 546–551.Google Scholar
Jeon, C.-J., Strettoi, E., & Masland, R.H. (1998). The major cell populations of the mouse retina. Journal of Neuroscience 18, 8936–8946.CrossRefGoogle Scholar
Johnson, P.T., Raven, M.A., & Reese, B.E. (2001). Disruption of transient photoreceptor targeting within the inner plexiform layer following early ablation of cholinergic amacrine cells in the ferret. Visual Neuroscience 18, 741–751.CrossRefGoogle Scholar
Kapfhammer, J.P., Christ, F., & Schwab, M.E. (1994). The expression of GAP-43 and synaptophysin in the developing rat retina. Developmental Brain Research 80, 251–260.CrossRefGoogle Scholar
Karlsen, R.L. (1978). The toxic effect of sodium glutamate and DL-alpha-aminoadipic acid on rat retina: Changes in high affinity uptake of putative transmitters. Journal of Neurochemistry 31, 1055–1061.CrossRefGoogle Scholar
Kim, I.-B., Lee, E.-J., Kim, M.-K., Park, D.-K., & Chun, M.-H. (2000). Choline acetyltransferase-immunoreactive neurons in the developing rat retina. Journal of Comparative Neurology 427, 604–616.3.0.CO;2-C>CrossRefGoogle Scholar
Linden, R. & Perry, V.H. (1982). Ganglion cell death within the developing retina: A regulatory role for retinal dendrites? Neuroscience 7, 2813–2837.Google Scholar
Lohmann, C. & Wong, R.O.L. (2001). Cell-type specific dendritic contacts between retinal ganglion cells during development. Journal of Neurobiology 48, 150–162.CrossRefGoogle Scholar
Lohmann, C., Myhr, K.L., & Wong, R.O. (2002). Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 418, 177–181.CrossRefGoogle Scholar
Marc, R. (1999a). Mapping glutamatergic drive in the vertebrate retina with a channel-permeant organic cation. Journal of Comparative Neurology 407, 47–64.Google Scholar
Marc, R. (1999b). Kainate activation of horizontal, bipolar, amacrine, and ganglion cells in the rabbit retina. Journal of Comparative Neurology 407, 65–76.Google Scholar
Millar, T.J. & Morgan, I.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281–285.CrossRefGoogle Scholar
Olney, J.W. (1968). An electron microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Investigative Ophthalmology 7, 250–268.Google Scholar
Olney, J.W. (1969). Glutamate-induced retinal degeneration in neonatal mice. Electron mocroscopy of the acutely evolving lesion. Journal of Neuropathology and Experimental Neurology 28, 455–474.CrossRefGoogle Scholar
Olney, J.W., Ho, O.L., & Rhee, V. (1971). Cytotoxic effects of acidic and sulphur containing amino acids on the infant mouse central nervous system. Experimental Brain Research 14, 61–76.Google Scholar
Park, J.-J., Oh, S.-J., Chung, J.-W., & Chun, M.-H. (2002). Tolerance of horizontal cells to excitotoxicity in the developing FVB/N mouse retina. NeuroReport 13, 2091–2095.CrossRefGoogle Scholar
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685.CrossRefGoogle Scholar
Raven, M.A. & Reese, B.E. (2002). Horizontal cell density and mosaic regularity in pigmented and albino mouse retina. Journal of Comparative Neurology 454, 168–176.CrossRefGoogle Scholar
Reese, B.E. & Galli-Resta, L. (2002). The role of tangential dispersion in retinal mosaic formation. Progress in Retinal and Eye Research 21, 153–168.CrossRefGoogle Scholar
Reese, B.E., Necessary, B.D., Tam, P.P.L., Faulkner-Jones, B., & Tan, S.-S. (1999). Clonal expansion and cell dispersion in the developing mouse retina. European Journal of Neuroscience 11, 2965–2978.CrossRefGoogle Scholar
Reese, B.E., Raven, M.A., Giannotti, K.A., & Johnson, P.T. (2001). Development of cholinergic amacrine cell stratification in the ferret retina and the effects of early excitotoxic ablation. Visual Neuroscience 18, 559–570.CrossRefGoogle Scholar
Rich, K.A., Zhan, Y., & Blanks, J.C. (1997). Migration and synaptogenesis of cone photoreceptors in the developing mouse retina. Journal of Comparative Neurology 388, 47–63.3.0.CO;2-O>CrossRefGoogle 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
Rossi, C., Strettoi, E., & Galli-Resta, L. (2003). The spatial order of horizontal cells is not affected by massive alterations in the organization of other retinal cells. Journal of Neuroscience 23, 9924–9928.Google Scholar
Sandmann, D., Engelmann, R., & Peichl, L. (1997). Starburst cholinergic amacrine cells in the tree shrew retina. Journal of Comparative Neurology 389, 161–176.3.0.CO;2-O>CrossRefGoogle Scholar
Schmidt, M., Wässle, H., & Humphrey, M. (1985). Number and distribution of putative cholinergic amacrine cells in cat retina. Neuroscience Letters 59, 235–240.CrossRefGoogle Scholar
Stacy, R.C. & Wong, R.O.L. (2003). Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina. Journal of Comparative Neurology 456, 154–166.CrossRefGoogle Scholar
Strettoi, E. & Volpini, M. (2002). Retinal organization in the bcl-2-overexpressing transgenic mouse. Journal of Comparative Neurology 446, 1–10.CrossRefGoogle 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, 101–119.CrossRefGoogle Scholar
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 2494–2501.CrossRefGoogle 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
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.CrossRefGoogle Scholar
Wässle, H., Boycott, B.B., & Illing, R.-B. (1981a). Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations. Proceedings of the Royal Society B (London) 212, 177–195.Google Scholar
Wässle, H., Peichl, L., & Boycott, B.B. (1981b). Morphology and topography of on- and off-alpha cells in the cat retina. Proceedings of the Royal Society B (London) 212, 157–175.Google Scholar
West Greenlee, M.H., Swanson, J.J., Simon, J.J., Elmquist, J.K., Jacobson, C.D., & Sakaguchi, D.S. (1996). Postnatal development and the differential expression of presynaptic terminal-associated proteins in the developing retina of the Brazilian opossum, Monodelphis domestica. Developmental Brain Research 96, 159–172.CrossRefGoogle Scholar
Wong, R.O.L. & Collin, S.P. (1989). Dendritic maturation of displaced putative cholinergic amacrine cells in the rabbit retina. Journal of Comparative Neurology 287, 164–178.CrossRefGoogle Scholar
Wong, R.O.L. & Ghosh, A. (2002). Activity-dependent regulation of dendritic growth and patterning. Nature Reviews Neuroscience 3, 803–812.CrossRefGoogle Scholar
Wong, W.T. & Wong, R.O. (2000). Rapid dendritic movements during synapse formation and rearrangement. Current Opinion in Neurobiology 10, 118–124.CrossRefGoogle Scholar
Yoon, Y.H., Jeong, K.H., Shim, M.J., & Koh, J.Y. (1999). High vulnerability of GABA-immunoreactive neurons to kainate in rat retinal cultures: Correlation with the kainate-stimulated cobalt uptake. Brain Research 823, 33–41.CrossRefGoogle Scholar
Zhang, C., Hammassaki-Britto, D.E., Britto, L.R.G., & Duvoisin, R.M. (1996). Expression of glutamate receptor subunit genes during development of the mouse retina. NeuroReport 8, 335–340.CrossRefGoogle Scholar