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Retinal projections in the cat: A cholera toxin B subunit study

Published online by Cambridge University Press:  22 January 2004

ISABELLE MATTEAU ,
DENIS BOIRE  and
MAURICE PTITO
ISABELLE MATTEAU
Affiliation:
Department of Psychology, University of Montreal, Canada, H3C 3J7 School of Optometry, University of Montreal, Canada, H3T 1P1
DENIS BOIRE
Affiliation:
School of Optometry, University of Montreal, Canada, H3T 1P1
MAURICE PTITO
Affiliation:
School of Optometry, University of Montreal, Canada, H3T 1P1
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Abstract

The B fragment of cholera toxin (CTb) is a highly sensitive anterograde tracer for the labelling of retinal axons. It can reveal dense retinofugal projections to well-known retinorecipient nuclei along with sparse but distinct input to target areas that are not commonly recognized. Following a unilateral injection of CTb into the vitreous chamber of seven adult cats, we localized the toxin immunohistochemically in order to identify direct retinal projections in these animals. Consistent with previous findings, the strongest projections were observed in the superficial layers of the superior colliculus, the dorsal and ventral lateral geniculate nuclei, the pretectal nuclei, the accessory optic nuclei, and the suprachiasmatic nucleus of the hypothalamus. However, we also found labelled terminals in several other brain areas, including the zona incerta, the medial geniculate nucleus, the lateral posterior-pulvinar complex, the lateral habenular nucleus, and the anterior and lateral hypothalamic regions. The morphological characteristics of the retinal axon terminals in most of the identified novel target sites are described.

Keywords

Retinal ganglion cellsVisionSubcortical visual pathwaysCarnivores
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 5 , September 2003 , pp. 481 - 493
Copyright
2003 Cambridge University Press

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References

REFERENCES

Agarwala, S., Petry, H.M., & May, J.G. (1989). Retinal projections in the ground squirrel (Citellus tridecemlineatus). Visual Neuroscience 3, 537–549.CrossRefGoogle Scholar
Angelucci, A., Clasca, F., & Sur, M. (1996). Anterograde axonal tracing with the subunit B of cholera toxin: A highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains. Journal of Neuroscience Methods 65, 101–112.CrossRefGoogle Scholar
Beckstead, R.M. & Frankfurter, A. (1983). A direct projection from the retina to the intermediate gray layer of the superior colliculus demonstrated by anterograde transport of horseradish peroxidase in monkey, cat, and rat. Experimental Brain Research 52, 261–268.Google Scholar
Berman, A.L. (1968). The Brain Stem of the Cat: A Cytoarchitectonic Atlas with Stereotaxic Coordinates. Madison, Wisconsin: University of Wisconsin Press.
Berman, N. (1977). Connections of the pretectum in the cat. Journal of Comparative Neurology 174, 227–254.CrossRefGoogle Scholar
Bhide, P.G. & Frost, D.O. (1991). Stages of growth of hamster retinofugal axons: Implications for developing axonal pathways with multiple targets. Journal of Neuroscience 11, 485–504.Google Scholar
Bhide, P.G. & Frost, D.O. (1999). Intrinsic determinants of retinal axon collateralization and arborization patterns. Journal of Comparative Neurology 411, 119–129.3.0.CO;2-W>CrossRefGoogle Scholar
Bowling, D.B. & Michael, C.R. (1984). Terminal patterns of single physiologically characterized optic tract fibers in cat. Nature 286, 899–902.Google Scholar
Brindley, G.S. & Hamasaki, D.I. (1962). Evidence that the cat's electroretinogram is not influenced by impulses passing to the eye along the optic nerve. Journal of Physiology 163, 558–565.CrossRefGoogle Scholar
Brindley, G.S. & Hamasaki, D.I. (1966). Histological evidence against the view that the cat's optic nerve contains centrifugal fibers. Journal of Physiology 184, 444–449.CrossRefGoogle Scholar
Brooke, R.N.L., Downer, J.C., & Powell, T.P.S. (1965). Centrifugal fibers to the retina in the monkey and cat. Nature 207, 1365–1367.CrossRefGoogle Scholar
Cooper, H.M., Mick, G., & Magnin, M. (1989). Retinal projection to mammalian telencephalon. Brain Research 477, 350–357.CrossRefGoogle Scholar
Cooper, H.M., Herbin, M., & Nevo, E. (1993). Visual system of a naturally microophthalmic mammal: The blind mole rat, Spalax ehrenbergi. Journal of Comparative Neurology 328, 313–350.CrossRefGoogle Scholar
Costa, M.S., Santee, U.R., Cavalcante, J.S., Moraes, P.R., Santos, N.P., & Britto, L.R. (1999). Retinohypothalamic projections in the common marmoset (Callithrix jacchus): A study using cholera toxin subunit B. Journal of Comparative Neurology 415, 393–403.3.0.CO;2-R>CrossRefGoogle Scholar
Derobert, Y., Medina, M., Rio, J.P., Ward, R., Reperant, J., Marchand, M.J., & Miceli, D. (1999). Retinal projections in two crocodilian species, Caiman crocodilus and Crocodylus niloticus. Anatomical Embryology (Berlin) 200, 175–191.CrossRefGoogle Scholar
Fite, K.V. & Janusonis, S. (2001). Retinal projection to the dorsal raphe nucleus in the Chilean degus (Octodon degus). Brain Research 895, 139–145.CrossRefGoogle Scholar
Foote, W., Taber-Pierce, E., & Edwards, L. (1978). Evidence for the retinal projection to the midbrain raphe of the cat. Brain Research 156, 135–140.CrossRefGoogle Scholar
Guillery, R.W., Geisert, E.E., Polley, E.H., & Mason, C.A. (1980). An analysis of the retinal afferents to the cat's medial intralaminar nucleus and to its rostral thalamic extension, the “geniculate wing”. Journal of Comparative Neurology 194, 117–142.CrossRefGoogle Scholar
Harting, J.K. & Guillery, R.W. (1976). Organization of retinocollicular pathways in the cat. Journal of Comparative Neurology 166, 133–144.CrossRefGoogle Scholar
Hayhow, W.R. (1959). An experimental study of the accessory optic fiber system in the cat. Journal of Comparative Neurology 113, 281–314.CrossRefGoogle Scholar
Hayhow, W.R. (1966). The accessory optic system in the marsupial phalanger, Trichosurus vulpecula. An experimental degeneration study. Journal of Comparative Neurology 126, 653–672.Google Scholar
Hayhow, W.R., Webb, C., & Jervie, A. (1960). The accessory optic fiber system in the rat. Journal of Comparative Neurology 115, 187–215.CrossRefGoogle Scholar
Higo, S. & Kawamura, S. (1999). Zonal organization of the ventral lateral geniculate nucleus in the cat: cholera toxin mapping. Journal of Comparative Neurology 415, 17–32.3.0.CO;2-F>CrossRefGoogle Scholar
Humphrey, A.L. & Weller, R.E. (1988). Structural correlates of functionally distinct X-cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 448–468.CrossRefGoogle Scholar
Hutchins, B. (1991). Evidence for a direct retinal projection to the anterior pretectal nucleus in the cat. Brain Research 561, 169–173.CrossRefGoogle Scholar
Hutchins, B. & Weber, J.T. (1985). The pretectal complex of the monkey: A reinvestigation of the morphology and retinal terminations. Journal of Comparative Neurology 232, 425–442.CrossRefGoogle Scholar
Itaya, S.K. & van Hoesen, G.W. (1982). Retinal innervation of the inferior colliculus in rat and monkey. Brain Research 233, 45–52.CrossRefGoogle Scholar
Itoh, K., Mizuno, N., & Kudo, M. (1983). Direct retinal projections to the lateroposterior and pulvinar nuclear complex (LP-Pul) in the cat, as revealed by anterograde HRP method. Brain Research 276, 325–328.CrossRefGoogle Scholar
Jhaveri, S., Edwards, M.A., & Schneider, G.E. (1991). Initial stages of retinofugal axon development in the hamster: Evidence for two distinct modes of growth. Experimental Brain Research 87, 371–382.Google Scholar
Johnson, R.F., Morin, L.P., & Moore, R.Y. (1988). Retinohypothalamic projections in hamsters and rats demonstrated using cholera toxin. Brain Research 462, 301–312.CrossRefGoogle Scholar
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319–334.CrossRefGoogle Scholar
Koontz, M.A., Rodieck, R.W., & Farmer, S.G. (1985). The retinal projection to the cat pretectum. Journal of Comparative Neurology 236, 42–59.CrossRefGoogle Scholar
Levine, J.D., Weiss, M.L., Rosenwasser, A.M., & Miselis, R.R. (1991). Retinohypothalamic tract in the female albino rat: A study using horseradish peroxidase conjugated to cholera toxin. Journal of Comparative Neurology 306, 344–360.CrossRefGoogle Scholar
Levine, J.D., Zhao, X.S., & Miselis, R.R. (1994). Direct and indirect retinohypothalamic projections to the supraoptic nucleus in the female albino rat. Journal of Comparative Neurology 341, 214–224.CrossRefGoogle Scholar
Ling, C., Schneider, G.E., Northmore, D., & Jhaveri, S. (1997). Afferents from the colliculus, cortex, and retina have distinct terminal morphologies in the lateral posterior thalamic nucleus. Journal of Comparative Neurology 388, 467–483.3.0.CO;2-Z>CrossRefGoogle Scholar
Ling, C., Schneider, G.E., & Jhaveri, S. (1998). Target-specific morphology of retinal axon arbors in the adult hamster. Visual Neuroscience 15, 559–579.Google Scholar
Magnin, M., Cooper, H.M., & Mick, G. (1989). Retinohypothalamic pathway: A breach in the law of Newton–Müller–Gudden? Brain Research 488, 390–397.Google Scholar
Mason, C.A. & Robson, J.A. (1979). Morphology of retino-geniculate axons in the cat. Neuroscience 4, 79–97.CrossRefGoogle Scholar
Mick, G., Cooper, H.M., & Magnin, M. (1993). Retinal projection to the olfactory tubercle and basal telencephalon in primates. Journal of Comparative Neurology 327, 205–219.CrossRefGoogle Scholar
Mikkelsen, J.D. (1992). Visualization of efferent retinal projections by immunohistochemical identification of cholera toxin subunit B. Brain Research Bulletin 28, 619–623.CrossRefGoogle Scholar
Moore, R.Y. (1973). Retinohypothalamic projection in mammals: A comparative study. Brain Research 49, 403–409.CrossRefGoogle Scholar
Moore, R.Y. & Lenn, N.J. (1972). A retino-hypthalamic projection in the rat. Journal of Comparative Neurology 146, 1–14.Google Scholar
Murakami, D.M., Miller, J.D., & Fuller, C.A. (1989). The retinohypothalamic tract in the cat: retinal ganglion cell morphology pattern of projection. Brain Research 482, 283–296.CrossRefGoogle Scholar
Nakagawa, S., Mizuma, M., & Kuchiiwas, S. (1998). The retinal projections to the ventral and dorsal divisions of the medial terminal nucleus and mesencephalic reticular formation in the Japanese monkey (Macaca fuscata): A reinvestigation with cholera toxin B subunit as a anterograde tracer. Brain Research 809, 198–203.CrossRefGoogle Scholar
Pickard, G.E. (1982). The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. Journal of Comparative Neurology 211, 65–83.CrossRefGoogle Scholar
Pickard, G.E. & Silverman, A.J. (1981). Direct retinal projections to the hypothalamus, piriform cortex, and accessory optic nuclei in the golden hamster as demonstrated by a sensitive anterograde horseradish peroxidase technique. Journal of Comparative Neurology 196, 155–172.CrossRefGoogle Scholar
Power, B.D., Leamey, C.A., & Mitrofanis, J. (2001). Evidence for a visual subsector within the zona incerta. Visual Neuroscience 18, 179–186.CrossRefGoogle Scholar
Qu, T., Dong, K., Sugioka, K., & Yamadori, T. (1996). Demonstration of direct input from the retina to the lateral habenular nucleus in the albino rat. Brain Research 709, 251–258.CrossRefGoogle Scholar
Reiner, A., Zhang, D., & Eldred, W.D. (1996). Use of the sensitive anterograde tracer cholera toxin fragment B reveals new details of the central retinal projections in turtles. Brain, Behavior, and Evolution 48, 307–337.Google Scholar
Reinoso-Suárez, F. (1961). Topographischer Hirnatlas der Katze. Darmstadt: Herausgegeben von E, Merck AG.
Robson, J.A. (1993). Qualitative and quantitative analyses of the pattern of retinal input to neurons in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 334, 324–336.CrossRefGoogle Scholar
Sur, M. & Sherman, S.M. (1982). Retinogeniculate terminations in cats: Morphological differences between physiologically identified X- and Y-cell axons. Science 218, 389–391.CrossRefGoogle Scholar
Sur, M., Esguerra, M., Garraghty, P.E., Kritzer, M.F., & Sherman, S.M. (1987). Morphology of physiologically identified retinogeniculate X- and Y-axons in the cat. Journal of Neurophysiology 58, 1–32.Google Scholar
Tamamaki, N., Uhlrich, D.J., & Sherman, S.M. (1995). Morphology of physiologically identified retinal X and Y axons in the cat's thalamus and midbrain as revealed by intraaxonal injection of biocytin. Journal of Comparative Neurology 354, 583–607.CrossRefGoogle Scholar
Weber, J.T. & Hutchins, B. (1982). The demonstration of a retinal projection to the medial pretectal nucleus in the domestic cat and the squirrel monkey: An autoradiographic analysis. Brain Research 232, 181–186.CrossRefGoogle Scholar
Youngstrom, T.G., Weiss, M.L., & Nunez, A.A. (1991). Retinofugal projections to the hypothalamus, anterior thalamus and basal forebrain in hamsters. Brain Research Bulletin 26, 403–411.CrossRefGoogle Scholar
Zhang, H.Y. & Hoffmann, K.P. (1993). Retinal projections to the pretectum, accessory optic system and superior colliculus in pigmented and albino ferrets. European Journal of Neuroscience 5, 486–500.CrossRefGoogle Scholar