Development of A-type (axonless) horizontal cells in the rabbit retina
Ronald Scheibe
Carl Ludwig Institute of Physiology, Leipzig University, D-04103 Leipzig, Federal Republic of Germany
Search for more papers by this authorJutta Schnitzer
Max Planck Institute for Brain Research, Department of Neuroanatomy, D-60528 Frankfurt am Main, Federal Republic of Germany
Search for more papers by this authorJürgen Röhrenbeck
Max Planck Institute for Brain Research, Department of Neuroanatomy, D-60528 Frankfurt am Main, Federal Republic of Germany
Search for more papers by this authorFrank Wohlrab
Pathological Institute, Leipzig University, D-04103 Leipzig, Federal Republic of Germany
Search for more papers by this authorCorresponding Author
Dr. Andreas Reichenbach
Carl Ludwig Institute of Physiology, Leipzig University, D-04103 Leipzig, Federal Republic of Germany
Carl Ludwig Institute of Physiology, Leipzig University, Liebigstrasse 27, D-04103 Leipzig, Federal Republic of GermanySearch for more papers by this authorRonald Scheibe
Carl Ludwig Institute of Physiology, Leipzig University, D-04103 Leipzig, Federal Republic of Germany
Search for more papers by this authorJutta Schnitzer
Max Planck Institute for Brain Research, Department of Neuroanatomy, D-60528 Frankfurt am Main, Federal Republic of Germany
Search for more papers by this authorJürgen Röhrenbeck
Max Planck Institute for Brain Research, Department of Neuroanatomy, D-60528 Frankfurt am Main, Federal Republic of Germany
Search for more papers by this authorFrank Wohlrab
Pathological Institute, Leipzig University, D-04103 Leipzig, Federal Republic of Germany
Search for more papers by this authorCorresponding Author
Dr. Andreas Reichenbach
Carl Ludwig Institute of Physiology, Leipzig University, D-04103 Leipzig, Federal Republic of Germany
Carl Ludwig Institute of Physiology, Leipzig University, Liebigstrasse 27, D-04103 Leipzig, Federal Republic of GermanySearch for more papers by this authorAbstract
The development of A-type horizontal cells (HC) was studied in the rabbit retina between embryonic day (E)24 and adulthood [the day of birth was called postnatal day (P)1 and corresponds to E31–32]. The cells were visualized by several methods 1) by immunolabeling with antibodies to neurofilament 70000 (NF-70kD), 2) by immunolabeling with antibodies to a calcium binding protein (CaBP-28kD), 3) by two different methods of silver impregnation, and (4) by histochemical demonstration of NADH-diaphorase activity. Most methods labeled A-type HC only in the dorsal retina; thus, our study is restricted to HC of this region. HC densities were determined at each developmental stage. The cells were drawn at scale, and size, quotient of symmetry, and topographical orientation of dendritic trees were studied by image analysis. The growth of HC dendritic fields was correlated with data on the postnatal local retinal expansion, which is known to be driven by the intraocular pressure (after cessation of retinal cell proliferation at P9). This expansion was evaluated in an earlier paper (Reichenbach et al. [1993] Vis. Neurosci. 10:479–498) by using local subpopulations of Müller cells as “markers” of distinct topographic regions of the retinae. After E24, when the final number of HC is established, we can discriminate three distinct developmental stages of A-type HC. During the first stage, between E24 and E27, the young cells are often vertically oriented and may extend their first short dendrites within (the primordia of) both plexiform layers. The irregular HC mosaic at E24 shows a significant difference to all other stages. The second stage begins after birth when the dendritic trees of the cells are already restricted to the outer plexiform layer. Between P3 and P9, their dendritic trees enlarge more than the surrounding retinal tissue expands, and the coverage factor almost doubles from 2.5 to 4.4. The third stage occurs after P9 when the growth rate of dendritic tree areas corresponds to that of the local retinal tissue expansion caused by “passive stretching” of the postmitotic tissue, and the coverage factor remains constant. This is compatible with the view that mature synaptic connections of A-type HC are mostly established after the first week of life and are then maintained. © 1995 Wiley-Liss, Inc.
Literature Cited
- Ahuja, N., and B. Schachter (1983) Pattern Models. New York: John Wiley & Sons.
- Ammermüller, J., W., Möckel, and P. Rujan (1993) A geometrical description of horizontal cell networks in the turtle retina. Brain Res. 616: 351–356.
- Araki, M., and H. Kimura (1991) GABA-like immunoreactivity in the developing chick retina: Differentiation of GABAergic horizontal cell and its possible contact with photoreceptors. J. Neurocytol. 20: 345–355.
- Bennett, G. S., and C. Di Lullo (1985) Transient expression of a neurofilament protein by replicating neuroepithelial cells of the embryonic chick brain. Dev. Biol. 107: 107–127.
- Bloomfield, S. A. (1992) A unique morphological subtype of horizontal cell in the rabbit retina with orientation-sensitive response properties. J. Comp. Neurol. 320: 69–85.
- Bloomfield, S. A., and R. F. Miller (1982) A physiological and morphological study of the horizontal cell types of the rabbit retina. J. Comp. Neurol. 208: 288–303.
- Bonfanti, L., P., Candeo, M. Piccinini, G. Carmignoto, M. C. Comelli, S. Ghindella, R. Bruno, A. Gobetto, and A. Merighi (1992) Distribution of protein gene product 9.5 (PGP 9.5) in the vertebrate retina: Evidence that immunoreactivity is restricted to mammalian horizontal and ganglion cells. J. Comp. Neurol. 322: 35–44.
- Boycott, B. B., and L. Peichl (1981) Neurofibrillar staining of cat retinae (Appendix to Peichl and Wässle, 1981). Proc. R. Soc. London [Biol.] 212: 153–156.
- Boycott, B. B., L., Peichl, and H. Wässle (1978) Morphological types of horizontal cell in the retina of the domestic cat. Proc. R. Soc. London [Biol.] 203: 229–245.
- Chu, Y., M. F., Humphrey, and I. J. Constable (1993) Horizontal cells of the normal and dystrophic rat retina: A wholemount study using immunolabelling for the 28-kDa calcium-binding protein. Exp. Eye Res. 57: 141–148.
-
Chun, M.-H., and
H. Wässle
(1993)
Some horizontal cells of the bovine retina receive input synapses in the inner plexiform layer.
Cell Tissue Res.
272:
447–457.
10.1007/BF00318551 Google Scholar
- Constantine-Paton, M., A. S., Blum, R. Mendez-Otero, and C. J. Barnstable (1986) A cell surface molecule distributed in a dorsoventral gradient in the perinatal rat retina. Nature 324: 459–462.
- Coulombre, A. J. (1956) The role of intraocular pressure in the development of the chick eye. J. Exp. Zool. 133: 211–223.
- Dacheux, R. F., and R. F. Miller (1981) An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. I. Receptors, horizontal, and bipolar cells. J. Comp. Neurol. 198: 307–326.
- Dacheux, R. F., and E. Raviola (1982) Horizontal cells in the retina of the rabbit. J. Neurosci. 2: 1486–1493.
- Deich, C., B., Seifert, L. Peichl, and A. Reichenbach (1994) Development of dendritic trees of rabbit retinal alpha ganglion cells: Relation to differential retinal growth. Vis. Neurosci. (in press).
- de Monasterio, F. M. (1978) Spectral interactions in horizontal and ganglion cells of the isolated and arterially-perfused rabbit retina. Brain Res. 150: 239–258.
- Dowling, J. E., J. E., Brown, and D. Major (1966) Synapses of horizontal cells in rabbit and cat retinas. Science 153: 1639–1641.
- Dräger, U. C. (1985) Neurofilaments in retinas of normal mice and of mice with hereditary photoreceptor loss. In J. B. Sheffield and S. R. Hilfer (eds): Heredity and Visual Development. New York: Springer-Verlag, pp. 43–62,
- Dräger, U. C., D. L., Edwards, and C. A. Barnstable (1984) Antibodies against filamentous components in discrete cell types of the mouse retina. J. Neurosci. 4: 2025–2042.
- Famiglietti, E. V. (1990) A new type of wide-field horizontal cell, presumably linked to blue cones, in rabbit retina. Brain Res. 535: 174–179.
- Fisher, S. K., and B. B. Boycott (1974) Synaptic connections made by horizontal cells within the outer plexiform layer of the retina of the cat and the rabbit. Proc. R. Soc. London [Biol.] 186: 317–331.
- Hinds, J. W., and P. L. Hinds (1974) Early ganglion cell differentiation in the mouse retina: An electron microscopic analysis utilizing serial sections. Dev. Biol. 37: 381–416.
- Hinds, J. W., and P. L. Hinds (1979) Differentiation of photoreceptors and horizontal cells in the embryonic mouse retina: An electron microscopic, serial section analysis. J. Comp. Neurol. 187: 495–512.
- Honrubia, F. M., and J. E. Elliott (1969) Horizontal cell of the mammal retina. Arch. Ophthalmol. 82: 98–104.
- Jansen, H. G., and S. Sanyal (1992) Synaptic plasticity in the rod terminals after partial photoreceptor cell loss in the heterozygous rds mutant mouse. J. Comp. Neurol. 316: 117–125.
- Kolb, H. (1974) The connections between horizontal cells and photoreceptors in the retina of the cat: Electron microscopy of Golgi preparations. J. Comp. Neurol. 155: 1–14.
- Kolb, H., and R. A. Norman (1982) A-type horizontal cells of the superior edge of the linear visual streak of the rabbit retina have oriented, elongated dendritic trees. Vis. Res. 22: 905–916.
- Kondo, H., M., Yamamoto, T. Yamakuni, and Y. Takahashi (1988) An immunohistochemical study of the ontogeny of the horizontal cell in the rat retina using an antiserum against spot 35 protein, a novel Purkinje cell-specific protein, as a marker. Anat. Rec. 222: 103–109.
- Leventhal, A. G., and J. D. Schall (1989) Extrinsic determinants of retinal ganglion cell development in cats and monkeys. In B. L. Finlay and D. R. Sengelaub (eds): Development of the Vertebrate Retina. New York: Plenum Press, pp. 173–195.
- Löhrke, S., J. H., Brandstätter, and L. Peichl (1993) Expression of the neurofilament triplet proteins in the rabbit retina. In N. Elsner and M. Heisenberg (eds): Gene-Brain-Behaviour. Stuttgart: Georg Thieme Verlag, p. 412.
- Löhrke, S., J. H., Brandstätter, B. B. Boycott, and L. Peichl (1995) Expression of neurofilament proteins by horizontal cells in the rabbit retina varies with retinal location. J. Neurocytol. (in press).
-
Lojda, Z.,
R., Gossrau, and
T. H. Schiebler
(1976)
Enzymhistochemische Methoden.
Berlin:
Springer.
10.1007/978-3-662-11693-7 Google Scholar
- Maslim, J., and J. Stone (1986) Synaptogenesis in the retina of the cat. Brain Res. 373: 35–48.
- Mastronarde, D. N., M. A., Thibeault, and M. W. Dubin (1984) Nonuniform postnatal growth of the cat retina. J. Comp. Neurol. 228: 598–608.
- McArdle, C. B., J. E., Dowling, and R. H. Masland (1977) Development of outer segments and synapses in the rabbit retina. J. Comp. Neurol. 175: 253–278.
- McCaffery, P., K. C., Posch, J. L. Napoli, L. Gudas, and U. C. Drager (1993) Changing patterns of the retinoic acid system in the developing retina. Dev. Biol. 158: 390–399.
- McCaffery, P., P., Tempst, G. Lara, and U. C. Dräger (1991) Aldehyde dehydrogenase is a positional marker in the retina. Development 112: 693–702.
- Mills, S. L., and S. C. Massey (1992) Morphology of bipolar cells labeled by DAPI in the rabbit retina. J. Comp. Neurol. 321: 133–149.
- Mills, S. L., and S. C. Massey (1994) Distribution and coverage of A- and B-type horizontal cells stained with neurobiotin in the rabbit retina. Vis. Neurosci. 11: 549–560.
- Mukai, N. (1975) A quick supra-vital staining method for the retinal Müller-fiber network under normal and pathological conditions. Brain Nerve 27: 545–549.
- Osborne, N., N., Patel, D. W. Beaton, and V. Neuhoff (1986) GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell Tissue Res. 243: 117–123.
- Peichl, L., and J. Bolz (1984) Kainic acid induces sprouting of retinal. Neurons. Science 223: 503–504.
- Peichl, L., and J. González-Soriano (1993) Unexpected presence of neurofilaments in axon-bearing horizontal cells of the mammalian retina. J. Neurosci. 13: 4091–4100.
- Peichl, L., and H. Wässle (1981) Morphological identification of on- and off-centre brisk transient (Y) cells in the cat retina. Proc. R. Soc. London [Biol.] 212: 139–153.[with an appendix by Boycott and Peichl (1981)].
- Perry, V. H., and L. Maffei (1988) Dendritic competition: Competition for what? Dev. Brain Res. 41: 195–208.
- Pradà, F., J. A., Armengol, and J. M. Génis-Gálvez (1984) Displaced horizontal cells in the chick retina. J. Morphol. 182: 221–225.
- Rabacchi, S. A., R. L., Neve, and U. C. Dräger (1990) A positional marker for the dorsal embryonic retina is homologous to the high-affinity laminin receptor. Development 109: 521–531.
- Ramoa, A. S., and Y. N. Yamasaki (1992) Mechanisms of dendritic tree development in mammalian retinal ganglion cells. In R. Lent (ed): The Visual System From Genesis to Maturity. New York: Birkhauser, pp. 71–85.
- Ramón y Cajal, S. (1893) La Rétine des Vertébrés. Cellule 9: 119–257.
- Ramón y Cajal, S. (1960) Development of the horizontal neurons in the mouse retina and their accidental alteration of location and direction. In L. Guth (transl): Studies of Vertebrate Neurogenesis. Springfield, IL: Charles C. Thomas, pp. 380–401.
- Raviola, E., and R. F. Dacheux (1983) Variations in structure and response properties of horizontal cells in the retina of the rabbit. Vis. Res. 23: 1221–1227.
- Raviola, E., and R. F. Dacheux (1990) Axonless horizontal cells of the rabbit retina: Synaptic connections and origin of the rod aftereffect. J. Neurocytol. 19: 731–736.
- Redburn, D. A., and P. Madtes- Jr. (1986) Postnatal development of 3H-GABAaccumulating cells in rabbit retina. J. Comp. Neurol. 243: 41–57.
- Reh, T. A., and T. Nagy (1989) Characterization of Rana germinal neuroepithelial cells in normal and regenerating retina. Neurosci. Res. Suppl. 10: S151–S162.
- Reh, T. A., W., Tetzlaff, A. Ertlmaier, and H. Zwiers (1993) Developmental study of the expression of B50/GAP-43 in rat retina. J. Neurobiol. 24: 949–958.
- Reichenbach, A. (1993) Two types of neuronal precursor cells in the mammalian retina—A short review. J. Hirnforsch. 34: 337–343.
- Reichenbach, A., and S. Pritz-Hohmeier (1994) Normal and disturbed early development of the eye anlagen. Progr. Eye Res. (in press).
- Reichenbach, A., and F. Wohlrab (1983) Horizontal cells of the rabbit retina: Some quantitative properties revealed by selective staining. Z. Mikrosk. Anat. Forsch. 97: 240–244.
- Reichenbach, A., W., Reichelt, and R. Schümann (1987) Use of Pappenheim's panoptic staining method on enzymatically isolated cells for demonstration of postnatal development of the rabbit retina. Z. Mikrosk. Anat. Forsch. 101: 597–608.
- Reichenbach, A., J., Schnitzer, A. Friedrich, W. Ziegert, G. Brückner, and W. Schober (1991a) Development of the rabbit retina. I. Size of eye and retina, and postnatal cell proliferation. Anat. Embryol. 183: 287–297.
- Reichenbach, A., J. Schnitzer, A. Friedrich, A.-K. Knothe, and A. Henke (1991b) Development of the rabbit retina. II. Müller cells, J. Comp. Neurol. 311: 33–44.
- Reichenbach, A., W. Eberhardtl R. Scheibe, C. Poich, B. Wert, W. Reichelt, K. Ddhnert, and M. Rödenbeck (1991c) Development of the rabbit retina. IV. Tissue tensility and elasticity in dependence on topographic special. Izations. Exp. Eye Res. 53: 241–251.
- Reichenbach, A., J., Schnitzer, E. Reichelt, N. N. Osborne, B. Fritzsche, A. Puls, U. Richter, A. Friedrich, K.-A. Knothe, W. Schober, and U. Timmermann (1993a) Development of the rabbit retina, III: Differential retinal growth, and density of projection neurons and interneurons. Vis. Neurosci. 10: 479–498.
- Reichenbach, A., J.-U., Stolzenburg, W. Eberhardt, T. I. Chao, D. Dettmer, and L. Hertz (1993b) What do retinal Müller (glial) cells do for their neuronal ‘small siblings’? J. Chem Neuroanat. 6: 201–213.
- Robinson, S. R. (1991) Development of the mammalian retina. In B. Dreher and S. R. Robinson (eds): Neuroanatomy of the Visual Pathways and Their Development. Vol. 3 of J. R. Cronly-Dillon (series ed): Vision and Visual Dysfunction. London: Macmillan, pp. 69–128.
- Robinson, S. R., B., Dreher, and M. J. McCall (1989) Nonuniform retinal expansion during the formation of the rabbit's visual streak: Implications for the ontogeny of mammalian retinal topography, Vis. Neurosci, 2: 201–219.
- Röhrenbeck, J., H., Wässle, and C. W. Heizmann (1987) Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neurosci. Lett. 77: 255–260.
- Röhrenbeck, J., H. Ädssle, and B. B. Boycott (1989) Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium binding proteins. Eur. J. Neurosci. 1: 407–420.
- Schnitzer, J., and A. C. Rusoff (1984) Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. J. Neurosci. 4: 2948–2955.
- Sechrist, J. W. (1968) Neurocytogenesis. I. Neurofibrils, neurofilaments, and the terminal mitotic cycle. Am. J. Anat. 124: 117–134.
- Shapiro, M. B., S. J. Schein, and F. M. De Monasterio (1985) Regularity and structure of the spatial pattern of blue cones of macaque retina. J. Am. Statist. Assoc. 80: 803–812.
- Shaw, G., and K. Weber (1983) The structure and development of the rat retina: An immunofluorescence microscopical study using antibodies specific for intermediate filament proteins. Eur. J. Cell Biol. 30: 219–232.
-
Silveira, L. C. L.,
E. S., Yamada, and
C. W. Picanco-Diniz
(1989)
Displaced horizontal cells and biplexiform horizontal cells in the mammalian retina.
Vis. Neurosci.
3:
483–488.
10.1017/S0952523800005988 Google Scholar
-
Sjöstrand, F. S.
(1976)
The outer plexiform layer of the rabbit retina, an important data processing center.
Vis. Res.
16:
1–14.
10.1016/0042-6989(76)90070-5 Google Scholar
- Sparrow, J. R., and C. J. Barnstable (1988) A gradient molecule in developing rat retina: Expression of 9-O-acetyl GD3 in relation to cell type, developmental age, and GD3 ganglioside. J. Neurosci. Res. 21: 398–409.
- Tapscott, S. J., G. S., Bennett, and H. Holtzer (1981) Neuronal precursor cells in the chick neural tube express neurofilament proteins. Nature 292: 836–837.
- Trisler, G. D., M. D., Schneider, and M. Nirenberg (1981) A topographic gradient of molecules in retina can be used to identify neuron position. Proc. Natl. Acad. Sci. USA 78: 2145–2149.
- Versaux-Botteri, C., R., Pochet, and J. Nguyen-Legros (1989) Immunohistochemical localization of GABA-containing neurons during postnatal development of the rat retina. Invest. Ophthalmol. Vis. Sci. 30: 652–659.