Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-24T01:00:54.010Z Has data issue: false hasContentIssue false
  • English
  • Français

A centrifugally controlled circuit in the avian retina and its possible role in visual attention switching

Published online by Cambridge University Press:  02 June 2009

Peter G.H. Clarke ,
Marcel Gyger  and
Stefan Catsicas
Peter G.H. Clarke
Affiliation:
Institute of Cell Biology and Morphology, University of Lausanne, Switzerland
Marcel Gyger
Affiliation:
Nestec Ltd., Nestlé Research Centre, Lausanne, Switzerland
Stefan Catsicas
Affiliation:
Institute of Cell Biology and Morphology, University of Lausanne, Switzerland
Get access Rights & Permissions [Opens in a new window]

Abstract

The isthmo-optic nucleus (ION) is the main source of efferents to the retina in birds. Isthmo-optic neurons project in topographical order on amacrine cells in the ventral parts of the retina, and a subclass of these known as proprioretinal neurons project onto the dorsal retina. We propose that, through the intermediary of the amacrine target cells, activity in the isthmo-optic pathway excites ganglion cells locally in the ventral retina but inhibits those in dorsal regions. This circuit would thereby mediate centrifugally controlled switches in attention between the dorsal retina, involved in feeding, and the more ventral parts, involved in scanning for predators. This hypothesis accounts for a wide range of disparate data from behavior, comparative anatomy, endocrinology, hodology, and neurophysiology.

Keywords

AttentionBirdsCentrifugal fibersIsthmo-optic nucleusVision
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 6 , November 1996 , pp. 1043 - 1048
Copyright
Copyright © Cambridge University Press 1996

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

Bagnoli, P., Fontanesi, G., Alesci, R. & Erichsen, J.T. (1992). Distribution of neuropeptide Y, substance P, and choline acetyltransferase in the developing visual system of the pigeon and effects of unilateral retina removal. Journal of Comparative Neurology 318, 392–414.CrossRefGoogle ScholarPubMed
Barfield, R.J., Ronay, G. & Pfaff, D.W. (1978). Autoradiographic localization of androgen-concentrating cells in the brain of the male domestic fowl. Neuroendocrinology 26, 297–311.CrossRefGoogle ScholarPubMed
Binggeli, R.L. & Paule, W.J. (1969). The pigeon retina: Quantitative aspects of the optic nerve and ganglion cell layer. Journal of Comparative Neurology 137, 1–18.Google Scholar
Brooks, B. & Holden, A.L. (1974). Centre and surround influences on the proximal negative response of the pigeon retina. Journal of Physiology (London) 239, 15–29.Google Scholar
Catsicas, S., Catsicas, M. & Clarke, P.G.H. (1987 a). Long-distance intraretinal connections in birds. Nature 326, 186–187.CrossRefGoogle ScholarPubMed
Catsicas, S., Thanos, S. & Clarke, P.G.H. (1987 b). Major role for neuronal death during brain development: Refinement of topographical connections. Proceedings of the National Academy of Sciences of the U.S.A. 84, 8165–8168.CrossRefGoogle ScholarPubMed
Clarke, P.G.H. & Whitteridge, D. (1976). The projection of the retina, including the ‘red area’ on to the optic tectum of the pigeon. Quarterly Journal of Experimental Physiology 61, 351–358.Google Scholar
Clarke, P.G.H. (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
Crossland, W.J. & Hughes, C.P. (1978). Observations on the afferent and efferent connections of the avian isthmo-optic nucleus. Brain Research 145, 239–256.Google Scholar
Ehrlich, D. (1981). Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer. Journal of Comparative Neurology 195, 643–657.Google Scholar
Ehrlich, D., Keyser, K.T. & Karten, H.J. (1987). Distribution of substance P-like immunoreactive retinal ganglion cells and their pattern of termination in the optic tectum of chick (Gallus gallus). Journal of Comparative Neurology 266, 220–233.Google Scholar
Feyerabend, B., Malz, C.R. & Meyer, D.L. (1994). Birds that feed-on-the-wing have few isthmo-optic neurons. Neuroscience Letters 182, 66–68.CrossRefGoogle ScholarPubMed
Fritzsch, B., Crapon de Caprona, M.D. & Clarke, P.G.H. (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 ScholarPubMed
Galifret, Y. (1968). Les diverses aires fonctionnelles de la rétine du Pigeon. Zeitschrift für Zellforschung 86, 535–545.CrossRefGoogle Scholar
Galifret, Y., Conde-Courtine, F., Repérant, J. & Servière, J. (1971). Centrifugal control in the visual system of the pigeon. Vision Research (Suppl.) 3, 185–200.Google Scholar
Gyger, M., Karakashian, S.J. & Marler, P. (1985). Avian alarm calling: Is there an audience effect? Animal Behavior 34, 1570–1572.CrossRefGoogle Scholar
Gyger, M., Karakashian, S.J., Dufty, A.M. Jr., & Marler, P. (1988). Alarm signals in birds: The role of testosterone. Hormones and Behavior 22, 305–314.CrossRefGoogle ScholarPubMed
Hahmann, U. & Güntürkün, O. (1992). Visual-discrimination deficits after lesions of the centrifugal visual system in pigeons (Columba livia). Visual Neuroscience 9, 225–233.Google 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
Holden, A.L. & Powell, T.P. (1972). The functional organization of the isthmo-optic nucleus in the pigeon. Journal of Physiology (London) 223, 419–447.Google Scholar
Holden, A.L. (1977 a). Concentric receptive fields of pigeon ganglion cells. Vision Research 17, 545–554.Google Scholar
Holden, A.L. (1977 b). Extensive lateral transmission in the inner plexiform layer of the pigeon retina. Vision Research 17, 665–666.CrossRefGoogle ScholarPubMed
Holden, A.L. (1990). Centrifugal pathways to the retina: Which way does the “searchlight” point? Visual Neuroscience 4, 493–495.CrossRefGoogle Scholar
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers in the pigeon retina. Science 150, 359–361.Google Scholar
McGill, J.I., Powell, T.P. & Cowan, W.M. (1966). The organization of the projection of the centrifugal fibres to the retina in the pigeon. Journal of Anatomy 100, 35–49.Google Scholar
McIlwain, J.T. (1964). Receptive fields of optic tract axons and lateral geniculate cells. Journal of Neurophysiology 27, 1154–1173.Google Scholar
Meyer, C.C., Parker, D.M. & Salzen, E.A. (1976). Androgensensitive midbrain sites and visual attention in chicks. Nature 259, 689–690.CrossRefGoogle ScholarPubMed
Miceli, D., Repérant, J., Rio, J.-P. & Medina, M. (1995). GABA immunoreactivity in the nucleus isthmo-opticus of the centrifugal visual system in the pigeon: A light and electron microscopic study. Visual Neuroscience 12, 425–441.CrossRefGoogle Scholar
Miles, F.A. (1972 a). Centrifugal control of the avian retina. 3. Effects of electrical stimulation of the isthmo-optic tract on the receptive field properties of retinal ganglion cells. Brain Research 48, 115–129.CrossRefGoogle ScholarPubMed
Miles, F.A. (1972 b). 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.CrossRefGoogle ScholarPubMed
Miles, F.A. (1972 c). Centrifugal control of the avian retina. II. Receptive field properties of cells in the isthmo-optic nucleus. Brain Research 48, 93–113.Google Scholar
Nickla, D.L., Gottlieb, M.D., Marin, G., Rojas, X., Britto, L.R.G. & Wallman, J. (1994). The retinal targets of centrifugal neurons and the retinal neurons projecting to the accessory optic system. Visual Neuroscience 11, 401–409.Google 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.CrossRefGoogle Scholar
Ramon Y Cajal, S. (1893). La rétine des vertébrés. La Cellule 9, 17–257.Google Scholar
Repérant, J., Miceli, D., Vesselkin, N.P. & Molotchnikoff, S. (1989). The centrifugal visual system of vertebrates: A century-old search reviewed. International Review of Cytology 118, 115–171.CrossRefGoogle ScholarPubMed
Rochon-Duvigneaud, A. (1943). Les yeux et la vision des vertébrés. Paris: Masson.Google Scholar
Rogers, L.J. & Miles, F.A. (1972). Centrifugal control of the avian retina. V. Effects of lesions of the isthmo-optic nucleus on visual behaviour. Brain Research 48, 147–156.Google Scholar
Rogers, L.J. & Andrew, R.J. (1989). Frontal and lateral visual field use by chicks after treatment with testosterone. Animal Behavior 38, 394–405.CrossRefGoogle Scholar
Schmid, H. (1995). Hirondelles et Martinets. Rapport de la Station ornithologique suisse de Sempach 1–37.Google Scholar
Shortess, G.K. & Klose, E.F. (1977). Effects of lesions involving efferent fibers to the retina in pigeons. Physiology and Behavior 18, 409–414.CrossRefGoogle Scholar
Uchiyama, H. & Watanabe, M. (1985). Tectal neurons projecting to the isthmo-optic nucleus in the Japanese quail. Neuroscience Letters 58, 381–385.Google Scholar
Uchiyama, H., Matsutani, S. & Watanabe, M. (1987). Activation of the isthmo-optic neurons by the visual Wulst stimulation. Brain Research 406, 322–325.Google Scholar
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.Google 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.Google 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 ScholarPubMed
Uchiyama, H., Ito, H. & Tauchi, M. (1995). Retinal neurones specific for centrifugal modulation of vision. Neuroreport 6, 889–892.Google Scholar
Weidner, C., Repérant, J., Desroches, A.M., Miceli, D. & Vesselkin, N.P. (1987). Nuclear origin of the centrifugal visual pathway in birds of prey. Brain Research 436, 153–160.Google Scholar
Woodson, W., Reiner, A., Anderson, K. & Karten, H.J. (1991). Distribution, laminar location, and morphology of tectal neurons projecting to the isthmo-optic nucleus and the nucleus isthmi, pars parvocellularis in the pigeon (Columba livia) and chick (Gallus domesticus): A retrograde labelling study. Journal of Comparative Neurology 305, 470–488.CrossRefGoogle 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.Google Scholar