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The composition of the inner nuclear layer of the cat retina

Published online by Cambridge University Press:  24 August 2009

MARGARET A. MacNEIL ,
SHERYL PURRIER  and
R. JARRETT RUSHMORE
MARGARET A. MacNEIL*
Affiliation:
Department of Biology, York College, CUNY, Jamaica, New York Biology Program, Graduate Center, CUNY, New York, New York
SHERYL PURRIER
Affiliation:
Department of Biology, York College, CUNY, Jamaica, New York
R. JARRETT RUSHMORE
Affiliation:
Laboratory of Cerebral Dynamics, Plasticity and Rehabilitation, Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachusetts
*
*Address correspondence and reprint requests to: Margaret A. MacNeil, Department of Biology, York College, CUNY, 94-20 Guy R. Brewer Boulevard, Jamaica, NY 11451. E-mail: [email protected]
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Abstract

The cellular composition of the inner nuclear layer (INL) is largely conserved among mammals. Studies of rabbit, monkey, and mouse retinas have shown that bipolar, amacrine, Müller, and horizontal cells make up constant fractions of the INL (42, 35, 20, and 3%, respectively); these proportions remain relatively constant at all retinal eccentricities. The purpose of our study was to test whether the organization of cat retina is similar to that of other mammalian retinas. Fixed retinas were embedded in plastic, serially sectioned at a thickness of 1 μm, stained, and imaged at high power in the light microscope. Bipolar, amacrine, Müller, and horizontal cells were classified and counted according to established morphological criteria. Additional sets of sections were processed for protein kinase C and calretinin immunoreactivity to determine the relative fraction of rod bipolar and AII amacrine cells. Our results show that the organization of INL in the cat retina contains species-specific alterations in the composition of the INL tied to the large fraction of rod photoreceptors. Compared with other mammalian retinas, cat retinas show an expansion of the rod pathway with rod bipolar cells accounting for about 70% of all bipolar cells and AII cells accounting for nearly a quarter of all amacrine cells. Our results suggest that evolutionary pressures in cats over time have refined their retinal organization to suit its ecological niche.

Keywords

Rod bipolar cellsAII amacrine cellsHorizontal cellsPhotoreceptorsImmunofluorescence
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 4 , July 2009 , pp. 365 - 374
Copyright
Copyright © Cambridge University Press 2009

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References

Ahnelt, P.K. & Kolb, H. (2000). The mammalian photoreceptor mosaic-adaptive design. Progress in Retinal and Eye Research 19, 711–777.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal and Eye Research 20, 351–384.CrossRefGoogle ScholarPubMed
Cohen, E. & Sterling, P. (1990). Demonstration of cell types among cone bipolar neurons of cat retina. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 330, 305–321.Google ScholarPubMed
Collin, S.P. & Pettigrew, J.D. (1988). Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high-density areae. Brain Behavior and Evolution 31, 283–295.CrossRefGoogle ScholarPubMed
Copenhagen, D.R., Hemila, S. & Reuter, T. (1990). Signal transmission through the dark-adapted retina of the toad (Bufo marinus). Gain, convergence, and signal/noise. The Journal of General Physiology 95, 717–732.CrossRefGoogle ScholarPubMed
Dyer, M.A., Martins, R., da Silva Filho, M., Muniz, J.A., Silveira, L.C.L., Cepko, C. & Finlay, B.L. (2009). Developmental sources of conservation and variation in the evolution of the primate eye. Proceedings of the National Academy of Sciences of the United States of America 106, 8963–8968.CrossRefGoogle ScholarPubMed
Freed, M.A., Smith, R.G. & Sterling, P. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. The Journal of Comparative Neurology 266, 445–455.CrossRefGoogle ScholarPubMed
Greferath, U., Grunert, U. & Wassle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. The Journal of Comparative Neurology 301, 433–442.CrossRefGoogle ScholarPubMed
Hughes, A. (1977). The topography of vision in mammals of contrasting life style: Comparative optics and retinal organisation. In Handbook of Sensory Physiology, ed. Crescitelli, F., pp. 615–756. Berlin, Germany: Springer-Verlag.Google Scholar
Jeon, C.J., Strettoi, E. & Masland, R.H. (1998). The major cell populations of the mouse retina. The Journal of Neuroscience 18, 8936–8946.CrossRefGoogle ScholarPubMed
Kavanau, J.L. (1970). Locomotion and activity phasing of 6 carnivores and a monkey. Experientia 26, 1026–1027.CrossRefGoogle Scholar
Kavanau, J.L. (1971). Locomotion and activity phasing of some medium-sized mammals. Journal of Mammalogy 52, 386–403.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 47–49.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.CrossRefGoogle ScholarPubMed
Kuwabara, N., Seki, K. & Aoki, K. (1986). Circadian, sleep and brain temperature rhythms in cats under sustained daily light-dark cycles and constant darkness. Physiology & Behavior 38, 283–289.CrossRefGoogle ScholarPubMed
Land, M.F. & Fernald, R.D. (1992). The evolution of eyes. Annual Review of Neuroscience 15, 1–29.CrossRefGoogle ScholarPubMed
Linberg, K., Cuenca, N., Ahnelt, P., Fisher, S. & Kolb, H. (2001). Comparative anatomy of major retinal pathways in the eyes of nocturnal and diurnal mammals. Progress in Brain Research 131, 27–52.CrossRefGoogle ScholarPubMed
Martin, P.R. & Grünert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. The Journal of Comparative Neurology 323, 269–287.CrossRefGoogle ScholarPubMed
Masland, R.H. (2001). The fundamental plan of the retina. Nature Neuroscience 4, 877–886.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in cat retina. The Journal of Neuroscience 4, 2920–2938.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1999). AII amacrine cells limit scotopic acuity in central macaque retina: A confocal analysis of calretinin labeling. The Journal of Comparative Neurology 411, 19–34.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Nathans, J. (1999). The evolution and physiology of human color vision: Insights from molecular genetic studies of visual pigments. Neuron 24, 299–312.CrossRefGoogle ScholarPubMed
NationalResearchCouncil, ed. (2003). Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research. Washington, DC: National Academies Press.Google Scholar
Petter, J.J. (1962). Ecological and behavioral studies of Madagascar lemurs in the field. Annals of the New York Academy of Sciences 102, 267–281.CrossRefGoogle ScholarPubMed
Rice, D.S. & Curran, T. (2000). Disabled-1 is expressed in type AII amacrine cells in the mouse retina. The Journal of Comparative Neurology 424, 327–338.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Ross, C.F. (2000). Into the light: The origin of Anthropoidea. Annual Review of Anthropology 29, 147–194.CrossRefGoogle Scholar
Steinberg, R.H., Reid, M. & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). The Journal of Comparative Neurology 148, 229–248.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cell. The Journal of Neuroscience 8, 623–642.CrossRefGoogle Scholar
Stone, J. (1983). Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. London: Plenum Press.CrossRefGoogle Scholar
Strettoi, E. & Masland, R.H. (1995). The organization of the inner nuclear layer of the rabbit retina. The Journal of Neuroscience 15, 875–888.CrossRefGoogle ScholarPubMed
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 United States of America 93, 14906–14911.CrossRefGoogle ScholarPubMed
Strettoi, E., Raviola, E. & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. The Journal of Comparative Neurology 325, 152–168.CrossRefGoogle ScholarPubMed
Strettoi, E. & Volpini, M. (2002). Retinal organization in the bcl-2-overexpressing transgenic mouse. The Journal of Comparative Neurology 446, 1–10.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1985). The morphology and topographic distribution of AII amacrine cells in the cat retina. Proceedings of the Royal Society of London. Series B, Biological Science 224, 475–488.Google ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, ed. Osborne, N.C.G., pp. 49–100. New York: Pergamon.Google Scholar
Vaney, D.I., Gynther, I.C. & Young, H.M. (1991). Rod-signal interneurons in the rabbit retina: 2. AII amacrine cells. The Journal of Comparative Neurology 310, 154–169.CrossRefGoogle ScholarPubMed
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews Neuroscience 5, 747–757.CrossRefGoogle ScholarPubMed
Wässle, H., Schafer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. The Journal of Neuroscience 6, 594–604.CrossRefGoogle ScholarPubMed
Williams, R.W., Cavada, C. & Reinoso-Suarez, F. (1993). Rapid evolution of the visual system: A cellular assay of the retina and dorsal lateral geniculate nucleus of the Spanish wildcat and the domestic cat. The Journal of Neuroscience 13, 208–228.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Hughes, A. (1987). Developing neuronal populations of the cat retinal ganglion cell layer. The Journal of Comparative Neurology 262, 473–495.CrossRefGoogle ScholarPubMed