Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-08T15:30:25.532Z Has data issue: false hasContentIssue false
  • English
  • Français

Association amacrine cells of Ramón y Cajal: Rediscovery and reinterpretation

Published online by Cambridge University Press:  03 February 2006

H. UCHIYAMA  and
W.K. STELL
H. UCHIYAMA
Affiliation:
Department of Information and Computer Science, Faculty of Engineering, Kagoshima University, Kagoshima, Japan
W.K. STELL
Affiliation:
Department of Cell Biology and Anatomy, University of Calgary Faculty of Medicine, Calgary, Alberta, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

In 1895, by means of the Golgi method, Santiago Ramón y Cajal discovered a cell having a unique morphology in the avian retina. This cell had its cell body in the amacrine cell level of the inner nuclear layer, only a few rudimentary dendrites at the outermost level of the inner plexiform layer (IPL), and a long axon coursing horizontally and terminating in the IPL. Despite having defined amacrine cells as cells without axons, Cajal named this cell type “association amacrine cell” (AAC). This discovery was not confirmed by other investigators for nearly a century. Very recently, however, isthmo-optic target cells (IOTCs), which receive the terminals of centrifugal fibers emanating from the isthmo-optic nucleus, have been identified as one type of AAC. As summarized and discussed in this review, the morphology of the AACs as described by Cajal has been completely confirmed. However, since these cells appear to be classical polarized, monoaxonal neurons and lack the dendritic interactions that are typical of amacrine cells, they should be regarded as a distinct type of retinal interneuron and not as amacrine cells.

Keywords

Ramón y CajalRetinaAssociation amacrine cellsIsthmo-optic nucleusCentrifugal modulation
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 6 , November 2005 , pp. 881 - 891
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Andres-Barquin, P.J. (2002). Santiago Ramon y Cajal and the Spanish school of neurology. Lancet Neurology 1, 445–452.CrossRefGoogle Scholar
Catsicas, S., Catsicas, M., & Clarke, P.G. (1987). Long-distance intraretinal connections in birds. Nature 326, 186–187.CrossRefGoogle Scholar
Chmielewski, C.E., Dorado, M.E., Quesada, A., Geniz-Galvez, J.M., & Prada, F.A. (1988). Centrifugal fibers in the chick retina. A morphological study. Anatomia Histologia Embryologia 17, 319–327.CrossRefGoogle Scholar
Clarke, P.G. (1992). Neuron death in the developing avian isthmo-optic nucleus, and its relation to the establishment of functional circuitry. Journal of Neurobiology 23, 1140–1158.CrossRefGoogle Scholar
Cowan, W.M. & Powell, T.P.S. (1963). Centrifugal fibers in the avian visual system. Proceedings of the Royal Society B 158, 232–252.CrossRefGoogle Scholar
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque monkey retina. Journal of Comparative Neurology 284, 275–293.CrossRefGoogle Scholar
DeFelipe, J. (2002). Sesquicentenary of the birthday of Santiago Ramon y Cajal, the father of modern neuroscience. Trends in Neuroscience 25, 481–484.CrossRefGoogle Scholar
Dogiel, A.S. (1895). Die Retina der Voegel. Archiv fur mikroskopische Anatomie 44, 622–646.CrossRefGoogle Scholar
Dowling, J.E. & Cowan, W.M. (1966). An electron microscope study of normal and degenerating centrifugal fiber terminals in the pigeon retina. Zeitschrift fur Zellforschung und Mikroskopisch Anatomia 71, 14–28.CrossRefGoogle Scholar
Fischer, A.J. & Stell, W.K. (1999). Nitric oxide synthase-containing cells in the retina, pigmented epithelium, choroid, and sclera of the chick eye. Journal of Comparative Neurology 405, 1–14.Google Scholar
Fritzsch, B., Crapon de Caprona, M.D., & Clarke, P.G. (1990). Development of two morphological types of retinopetal fibers in chick embryos, as shown by the diffusion along axons of a carbocyanine dye in the fixed retina. Journal of Comparative Neurology 300, 405–421.CrossRefGoogle Scholar
Hayes, B.P. & Holden, A.L. (1983). The distribution of centrifugal terminals in the pigeon retina. Experimental Brain Research 49, 189–197.Google Scholar
Hayes, B.P. & Webster, K.E. (1981). Neurones situated outside the isthmo-optic nucleus and projecting to the eye in adult birds. Neuroscience Letters 26, 107–112.CrossRefGoogle Scholar
Holden, A.L. & Powell, T.P. (1972). The functional organization of the isthmo-optic nucleus in the pigeon. Journal of Physiology 223, 419–447.CrossRefGoogle Scholar
Hu, J., Li, S., Xiao, Q., & Wang, S.R. (2001). Tecto-isthmo-optic transmission in pigeons is mediated by glutamate and nitric oxide. Brain Research Bulletin 54, 399–403.CrossRefGoogle Scholar
Li, J.L., Xiao, Q., Fu, Y.X., & Wang, S.R. (1998). Centrifugal innervation modulates visual activity of tectal cells in pigeons. Visual Neuroscience 15, 411–415.Google Scholar
Mariani, A.P. (1982). Association amacrine cells could mediate directional selectivity in pigeon retina. Nature 298, 654–655.CrossRefGoogle Scholar
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers in the pigeon retina. Science 150, 359–361.CrossRefGoogle Scholar
Medina, M., Reperant, J., Miceli, D., Bertrand, C., & Bennis, M. (1998). An immunohistochemical study of putative neuromodulators and transmitters in the centrifugal visual system of the quail (Coturnix japonica). Journal of Chemical Neuroanatomy 15, 75–95.CrossRefGoogle Scholar
Miceli, D., Reperant, J., Bavikati, R., Rio, J.P., & Volle, M. (1997). Brain-stem afferents upon retinal projecting isthmo-optic and ectopic neurons of the pigeon centrifugal visual system demonstrated by retrograde transneuronal transport of rhodamine beta-isothiocyanate. Visual Neuroscience 14, 213–224.CrossRefGoogle Scholar
Miceli, D., Reperant, J., Rio, J.P., Hains, P., & Medina, M. (2002). Serotonin immunoreactivity in the retinal projecting isthmo-optic nucleus and evidence of brainstem raphe connections in the pigeon. Brain Research 958, 122–129.CrossRefGoogle Scholar
Miles, F.A. (1972a). Centrifugal control of the avian retina. II. Receptive field properties of cells in the isthmo-optic nucleus. Brain Research 48, 93–113.Google Scholar
Miles, F.A. (1972b). Centrifugal control of the avian retina. III. Effects of electrical stimulation of the isthmo-optic tract on the receptive field properties of retinal ganglion cells. Brain Research 48, 115–129.Google Scholar
Miles, F.A. (1972c). Centrifugal control of the avian retina. IV. Effects of reversible cold block of the isthmo-optic tract on the receptive field properties of cells in the retina and isthmo-optic nucleus. Brain Research 48, 131–145.Google Scholar
Morgan, I.G., Miethke, P., & Li, Z.K. (1994). Is nitric oxide a transmitter of the centrifugal projection to the avian retina? Neuroscience Letters 168, 5–7.Google Scholar
Nickla, D.L., Gottlieb, M.D., Marin, G., Rojas, X., Britto, L.R., & Wallman, J. (1994). The retinal targets of centrifugal neurons and the retinal neurons projecting to the accessory optic system. Visual Neuroscience 11, 401–409.CrossRefGoogle Scholar
O'Leary, D.D. & Cowan, W.M. (1982). Further studies on the development of the isthmo-optic nucleus with special reference to the occurrence and fate of ectopic and ipsilaterally projecting neurons. Journal of Comparative Neurology 212, 399–416.CrossRefGoogle Scholar
Pearlman, A.L. & Hughes, C.P. (1976). Functional role of efferents to the avian retina. II. Effects of reversible cooling of the isthmo-optic nucleus. Journal of Comparative Neurology 166, 123–131.Google Scholar
Piccolino, M. (1988). Cajal and the retina: A 100-year retrospective. Trends in Neuroscience 11, 521–525.CrossRefGoogle Scholar
Ramón y Cajal, S. (1889). Sur la morphologie et les connexions des elements de la retine des oiseaux. Anatomischer Anzeiger 4, 111–121.Google Scholar
Ramón y Cajal, S. (1893). La rétine des vertébrés. La Cellule 9, 119–257.Google Scholar
Ramón y Cajal, S. (1894). Die Retina der Wirbelthiere. Wiesbaden: J.F. Bergmann.
Ramón y Cajal, S. (1895). Sobre unos corpúsculos especiales de la retina de las aves. Actas de la Sociedad Española de Historia Natural 24, 128–130.Google Scholar
Ramón y Cajal, S. (1896). Nouvelles contributions à l'étude histologique de la rétine. Journal de l'Anatomie et de la Physiologie 32, 481–543.Google Scholar
Ramón y Cajal, S. ( 1899–1904). Textura del sistema nervioso del hombre y vertebrados. Madrid: Moya.
Ramón y Cajal, S. (1909–1911). Histologie du systéme nerveux de l'homme et des vertebras. Madrid: Moya.
Ramón y Cajal, S. (1933). La rétine des vertébrés. Madrid: XIV Concilium Ophthalmologicum.
Ramón y Cajal, S. (1967). The structure and connexions of neurons. In Nobel Lectures, Physiology or Medicine 1901–1921, pp. 220–253. Amsterdam: Elsevier.
Ramón y Cajal, S. (1972). The Structure of the Retina. Springfield: Charles C. Thomas.
Ramón y Cajal, S. (1973). The vertebrate retina. In The Vertebrate Retina, ed. Rodieck, R.W., pp. 775–904. San Francisco, California: W.H. Freeman.
Ramón y Cajal, S. (1989). Recollections of My Life. Cambridge, Massachusetts: MIT Press.
Ramón y Cajal, S. (1995). Histology of the Nervous System. New York: Oxford University Press.
Ramón y Cajal, S. (1999–2002). Texture of the Nervous System of Man and the Vertebrates. New York: Springer.
Rensink, R.A. (2000). Seeing, sensing, and scrutinizing. Vision Research 40, 1469–1487.CrossRefGoogle Scholar
Sanna, P.P., Keyser, K.T., Deerink, T.J., Ellisman, M.H., Karten, H.J., & Bloom, F.E. (1992). Distribution and ontogeny of parvalbumin immunoreactivity in the chicken retina. Neuroscience 47, 745–751.CrossRefGoogle Scholar
Sotelo, C. (2003). Viewing the brain through the master hand of Ramon y Cajal. Nature Review Neuroscience 4, 71–77.CrossRefGoogle Scholar
Treisman, A. (1986). Features and objects in visual processing. Scientific American 255, 114–125.CrossRefGoogle Scholar
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
Uchiyama, H. (1999). The isthmo-optic nucleus: A possible neural substrate for visual competition. Neurocomputing 26–7, 565–571.CrossRefGoogle Scholar
Uchiyama, H., Aoki, K., Yonezawa, S., Arimura, F., & Ohno, H. (2004). Retinal target cells of the centrifugal projection from the isthmo-optic nucleus. Journal of Comparative Neurology 476, 146–153.CrossRefGoogle Scholar
Uchiyama, H. & Barlow, R.B. (1994). Centrifugal inputs enhance responses of retinal ganglion cells in the Japanese quail without changing their spatial coding properties. Vision Research 34, 2189–2194.CrossRefGoogle Scholar
Uchiyama, H. & Ito, H. (1993). Target cells for the isthmo-optic fibers in the retina of the Japanese quail. Neuroscience Letters 154, 35–38.CrossRefGoogle Scholar
Uchiyama, H., Ito, H., & Tauchi, M. (1995). Retinal neurones specific for centrifugal modulation of vision. NeuroReport 6, 889–892.CrossRefGoogle Scholar
Uchiyama, H., Matsutani, S., & Watanabe, M. (1987). Activation of the isthmo-optic neurons by the visual Wulst stimulation. Brain Research 406, 322–325.CrossRefGoogle Scholar
Uchiyama, H., Nakamura, S., & Imazono, T. (1998). Long-range competition among the neurons projecting centrifugally to the quail retina. Visual Neuroscience 15, 417–423.Google Scholar
Uchiyama, H., Yamamoto, N., & Ito, H. (1996). Tectal neurons that participate in centrifugal control of the quail retina: a morphological study by means of retrograde labeling with biocytin. Visual Neuroscience 13, 1119–1127.CrossRefGoogle Scholar
Vaney, D.I. (2002). Retinal neurons: Cell types and coupled networks. Progress in Brain Research 136, 239–254.CrossRefGoogle Scholar
Volgyi, B., Xin, D., Amarillo, Y., & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. Journal of Comparative Neurology 440, 109–125.CrossRefGoogle Scholar
Von Bartheld, C.S. & Johnson, J.E. (2001). Target-derived BDNF (brain-derived neurotrophic factor) is essential for the survival of developing neurons in the isthmo-optic nucleus. Journal of Comparative Neurology 433, 550–564.CrossRefGoogle Scholar
Wallenberg, A. (1898). Das mediale Opticusbündel der Taube. Neurol Zbl 17, 532–537.Google Scholar
Woodson, W., Shimizu, T., Wild, J.M., Schimke, J., Cox, K., & Karten, H.J. (1995). Centrifugal projections upon the retina: An anterograde tracing study in the pigeon (Columba livia). Journal of Comparative Neurology 362, 489–509.CrossRefGoogle Scholar