Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-02T18:27:52.710Z Has data issue: false hasContentIssue false

Interlaminar connections of the superior colliculus in the tree shrew. II: Projections from the superficial gray to the optic layer

Published online by Cambridge University Press:  02 June 2009

Psyche Lee
Affiliation:
Department of Neurobiology, Duke University, Durham
William C. Hall
Affiliation:
Department of Neurobiology, Duke University, Durham

Abstract

This study of the tree shrew, Tupaia belangeri, provides evidence for an intracollicular pathway that arises in the superficial gray layer and terminates in the optic layer. As a first step, Nissl, myelin, and cytochrome oxidase stains were used to identify the layers of the superior colliculus in the tree shrew. Second, anterograde and retrograde axonal transport methods were used to determine relationships between laminar borders and patterns of connections. Intraocular injections of wheat germ agglutinin conjugated to horseradish peroxidase showed that the border between the superficial gray and optic layers in the tree shrew is marked by a sharp decrease in the density of retinotectal projections. The optic layer also could be distinguished from the subjacent intermediate gray layer by differences in connections. Of the two layers, only the intermediate gray layer received projections following injections of wheat germ agglutinin conjugated to horseradish peroxidase within substantia nigra pars reticulata. Similarly, following injections of horseradish peroxidase or biocytin in the paramedian pons, the intermediate gray but not the optic layer contained labeled cells of origin for the main premotor pathway from the tectum, the predorsal bundle. Next, cells in the superficial gray layer were intracellularly injected with biocytin in living brain slices. Axons were traced from narrow and wide field vertical cells in the deep part of the superficial gray layer to the gray matter surrounding the fiber fascicles of the optic layer. Small extracellular injections of biocytin in brain slices showed that the optic layer gray matter contains a population of stellate cells that are in position to receive the input from the superficial layer. Finally, small extracellular injections of biocytin in the intermediate gray layer filled cells that sent prominent apical dendrites into the optic layer, where they may be directly contacted by the superficial gray layer cells. Taken together, the results support the hypothesis that the optic layer is functionally distinct from its adjacent layers, and may provide a link in the transfer of information from the superficial, retinal recipient, to the intermediate, premotor, layer of the superior colliculus.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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

Abplanalp, P. (1970). Some subcortical connections of the visual system in tree shrews and squirrels. Brain, Behavior, and Evolution 3, 155168.Google ScholarPubMed
Adams, J.C. (1981). Heavy metal intensification of DAB-based reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Aghajanian, O.K. & Rasmussen, K. (1989). Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3, 331338.CrossRefGoogle ScholarPubMed
Albano, J.E., Norton, T.T. & Hall, W.C. (1979). Laminar origin of projections from the superficial layers of the superior colliculus in the tree shrew, Tupaia glis. Brain Research 173, 111.CrossRefGoogle ScholarPubMed
Beckstead, R.M. & Frankfurter, A. (1983). A direct projection from the retina to the intermediate grey layer of the superior colliculus demonstrated by anterograde transport of horseradish peroxidase in monkey, cat and rat. Experimental Brain Research 52, 261268.CrossRefGoogle Scholar
Behan, M. (1981). Identification and distribution of retinocollicular terminals in the cat: An electron-microscopic autoradiographic analysis. Journal of Comparative Neurology 199, 115.CrossRefGoogle Scholar
Behan, M. (1984). An EM-autoradiographic analysis of the projection from cortical areas 17, 18 and 19 to the superior colliculus in the cat. Journal of Comparative Neurology 225, 591604.CrossRefGoogle Scholar
Behan, M. & Appell, P.P. (1992). Intrinsic circuitry in the cat superior colliculus: Projections from the superficial layers. Journal of Comparative Neurology 315, 230243.CrossRefGoogle ScholarPubMed
Berson, D.M. & McIlwain, J.T. (1982). Retinal Y-cell activation of deep-layer cet's in superior colliculus of the cat. Journal of Neurophysiology 47, 700714.CrossRefGoogle Scholar
Berson, D.M. & McIlwain, J.T. (1983). Visual cortical inputs to deep layers of cat's superior colliculus. Journal of Neurophysiology 50, 11431155.CrossRefGoogle ScholarPubMed
Bickford, M.E. & Hall, W.C. (1989). Collateral projections of pre-dorsal bundle cells of the superior colliculus in the rat. Journal of Comparative Neurology 283, 86106.CrossRefGoogle Scholar
Caldwell, R.B. & Mize, R.R. (1981). Superior colliculus neurons which project to the cat lateral posterior nucleus have varying morphologies. Journal of Comparative Neurology 203, 5366.CrossRefGoogle Scholar
Casseday, J.H., Jones, D.R. & Diamond, I.T. (1979). Projections from cortex to tectum in the tree shrew, Tupaia glis. Journal of Comparative Neurology 185, 253292.CrossRefGoogle ScholarPubMed
Chalupa, L.M. & Rhoades, R.W. (1979). An autoradiographic study of the retinotectal projection in the golden hamster. Journal of Comparative Neurology 186, 561570.CrossRefGoogle ScholarPubMed
Donnelly, J.F., Thompson, S.M. & Robertson, R.T. (1983). Organization of projections from the superior colliculus to the thalamic lateral posterior nucleus in the rat. Brain Research 288, 315319.CrossRefGoogle Scholar
Graham, J. & Casagrande, V.A. (1980). A light microscopic and electron microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis). Journal of Comparative Neurology 191, 133151.CrossRefGoogle ScholarPubMed
Graham, J., Lin, C.-S. & Kaas, J.H. (1979). Subcortical projections of six visual cortical areas in the owl monkey, Aotus trivirgatus. Journal of Comparative Neurology 187, 557580.CrossRefGoogle ScholarPubMed
Grantyn, R., Ludwig, R. & Eberhardt, W. (1984). Neurons of the superficial tectal gray. An intracellular HRP-study of the kitten superior colliculus in vitro. Experimental Brain Research 55, 172176.CrossRefGoogle Scholar
Graybiel, A.M. (1975). Anatomical organization of retinotectal afferents in the cat: An autoradiographic study. Brain Research 96, 123.CrossRefGoogle Scholar
Hall, W.C. & Lee, P. (1993). Interlaminar connections of the superior colliculus in the tree shrew. I. The superficial gray layer. Journal of Comparative Neurology 332, 213223.CrossRefGoogle ScholarPubMed
Harting, J.K., Casagrande, V.A. & Weber, J.T. (1978). The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: Autoradiographic demonstration of interlaminar distribution of tectogeniculate axons. Brain Research 150, 593599.CrossRefGoogle ScholarPubMed
Harting, J.K. & Guillery, R.W. (1976). Organization of retinocollicular pathways in the cat. Journal of Comparative Neurology 166, 133144.CrossRefGoogle ScholarPubMed
Harting, J.K. & Noback, C.R. (1971). Subcortical projections from the visual cortex in the tree shrew (Tupaia glis). Brain Research 25, 2133.CrossRefGoogle ScholarPubMed
Harting, J.K., Updyke, B.V. & Van Lieshout, D.P. (1992). Corticotectal projections in the cat: Anterograde transport studies of twenty-five cortical areas. Journal of Comparative Neurology 324, 379414.CrossRefGoogle ScholarPubMed
Hofbauer, A. & Drager, U.C. (1985). Depth segregation of retinal ganglion cells projecting to mouse superior colliculus. Journal of Comparative Neurology 234, 465474.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. (1973). Conduction velocity in pathways from retina to superior colliculus in the cat: A correlation with receptive-field properties. Journal of Neurophysiology 36, 409424.CrossRefGoogle Scholar
Holcombe, V. & Hall, W.C. (1981). The laminar origin and distribution of the crossed tectoreticular pathways. Journal of Neuroscience 1, 11031112.CrossRefGoogle ScholarPubMed
Hubel, D.H. (1975). An autoradiographic study of the retino-cortical projections in the tree shrew (Tupaia glis). Brain Research 96, 4150.CrossRefGoogle ScholarPubMed
Hubel, D.H., Levay, S. & Wiesel, T.N. (1975). Mode of termination of retinotectal fibers in Macaque monkey: An autoradiographic study. Brain Research 96, 2540.CrossRefGoogle ScholarPubMed
Huerta, M.F. & Harting, J.K. (1983). Sublamination within the superficial gray layer of the squirrel monkey: An analysis of the tecto-pulvinar projection using anterograde and retrograde transport methods. Brain Research 261, 119126.CrossRefGoogle Scholar
Katz, L.C. (1987). Local circuitry of identified projection neurons in cat visual cortex brain slices. Journal of Neuroscience 7, 12231249.CrossRefGoogle ScholarPubMed
Kawamura, K. & Hashikawa, T. (1978). Cell bodies of origin of reticular projections from the superior colliculus in the cat: An experimental study with the use of horseradish peroxidase as a tracer. Journal of Comparative Neurology 182, 116.CrossRefGoogle Scholar
Kawamura, S., Fukushtma, N., Hattori, S. & Kudo, M. (1980). Laminar segregation of cells of origin of ascending projections from the superficial layers of the superior colliculus in the cat. Brain Research 184, 486490.CrossRefGoogle ScholarPubMed
Kawamura, S. & Kobayashi, E. (1975). Identification of laminar origin of some tecto-thalamic fibers in the cat. Brain Research 91, 281285.CrossRefGoogle ScholarPubMed
Langer, T.P. & Lund, R.D. (1974). The upper layers of the superior colliculus of the rat: A Golgi study. Journal of Comparative Neurology 158, 405436.CrossRefGoogle Scholar
Ma, T.P., Graybiel, A.M. & Wurtz, R.H. (1991). Location of saccade-related neurons in the macaque superior colliculus. Experimental Brain Research 85, 2135.CrossRefGoogle ScholarPubMed
May, P.J. & Hall, W.C. (1984). Relationships between the nigrotectal pathway and the cells of origin of the predorsal bundle. Journal of Comparative Neurology 226, 357376.CrossRefGoogle ScholarPubMed
May, P.J. & Porter, J.D. (1992). The laminar distribution of macaque tectobulbar and tectospinal neurons. Visual Neuroscience 8, 257276.CrossRefGoogle ScholarPubMed
Mays, L.E. & Sparks, D.L. (1980). Dissociation of visual and saccade-related responses in superior colliculus neurons. Journal of Neurophysiology 43, 207232.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1976). Large receptive fields and spatial transformations in the visual system. In International Review of Physiology, ed. Porter, R., pp. 223248. Baltimore, MD: University Park Press.Google Scholar
McIlwain, J.T. & Lufkin, R.B. (1976). Distribution of direct Y-cell inputs to the cat's superior colliculus: are there spatial gradients? Brain Research 103, 133138.CrossRefGoogle Scholar
Mize, R.R. (1983). Patterns of convergence and divergence of retinal and conical synaptic terminals in the cat superior colliculus. Experimental Brain Research 51, 8896.CrossRefGoogle Scholar
Mohler, C.W. & Wurtz, R.H. (1976). Organization of monkey superior colliculus: Intermediate layer cells discharging before eye movements. Journal of Neurophysiology 39, 722744.CrossRefGoogle ScholarPubMed
Mooney, R.D., Klein, B.C., Jacquin, M.F. & Rhoades, R.W. (1984). Dendrites of deep layer, somatosensory superior collicular neurons extend into the superficial laminae. Brain Research 324, 361365.CrossRefGoogle ScholarPubMed
Mooney, R.D., Nikoletseas, M.M., Hess, P.R., Allen, Z., Lewin, A.C. & Rhoades, R.W. (1988 a). The projection from the superficial to the deep layers of the superior colliculus: An intracellular horseradish peroxidase injection study in the hamster. Journal of Neuroscience 8, 13841399.CrossRefGoogle Scholar
Mooney, R.D., Nikoletseas, M.M., Ruiz, S.A. & Rhoades, R.W. (1988 b). Receptive-field properties and morphological characteristics of the superior colliculus neurons that project to the lateral posterior and dorsal lateral geniculate nuclei in the hamster. Journal of Neurophysiology 59, 13331351.CrossRefGoogle Scholar
Mooney, R.D. & Rhoades, R.W. (1990). Relationships between physiological and morphological properties of retinocollicular axons in the hamster. Journal of Neuroscience 10, 31643177.CrossRefGoogle ScholarPubMed
Moschovakis, A.K. & Karabelas, A.B. (1985). Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat. Journal of Comparative Neurology 239, 276308.CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. (1988 a). Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. Journal of Neurophysiology 60, 232262.CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. (1988 b). Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. Journal of Neurophysiology 60, 263302.CrossRefGoogle ScholarPubMed
Norita, M. (1980). Neurons and synaptic patterns in the deep layers of the superior colliculus of the cat. A Golgi and electron-microscopic study. Journal of Comparative Neurology 190, 2948.CrossRefGoogle Scholar
Ogawa, T. & Takahashi, Y. (1981). Retinotectal connectivities within the superficial layers of the cat's superior colliculus. Brain Research 217, 111.CrossRefGoogle ScholarPubMed
Olivier, E., Chat, M. & Grantyn, A. (1991). Rostrocaudal and lateromedial density distributions of superior colliculus neurons projecting in the predorsal bundle and to the spinal cord: A retrograde HRP study in the cat. Experimental Brain Research 87, 268282.CrossRefGoogle Scholar
Ramón Y Cajal, S. (1911). Histologie du Système Nerveux de l'Homme et des Vertébrés, Vol. II. Paris: Maloine.Google Scholar
Redgrave, P., Odekunle, A. & Dean, P. (1986). Tectal cells of origin of predorsal bundle in rat: Location and segregation from ipsilateral descending pathway. Experimental Brain Research 63, 279293.CrossRefGoogle ScholarPubMed
Rhoades, R.W. (1981). Expansion of the ipsilateral visual corticotectal projection in hamsters subjected to partial lesions of the visual cortex during infancy: Anatomical experiments. Journal of Comparative Neurology 197, 425445.CrossRefGoogle ScholarPubMed
Rhoades, R.W. & Chalupa, L.M. (1978). Functional and anatomical consequences of neonatal visual cortical damage in superior colliculus of the golden hamster. Journal of Neurophysiology 41, 14661494.CrossRefGoogle ScholarPubMed
Rhoades, R.W., Mooney, R.D., Klein, E.G., Jacquin, M.F., Szczepanik, A.M. & Chiaia, N.L. (1987). The structural and functional characteristics of tectospinal neurons in the golden hamster. Journal of Comparative Neurology 255, 451465.CrossRefGoogle ScholarPubMed
Rhoades, R.W., Mooney, R.D., Rohrer, W.H., Nikoletseas, M.M. & Fish, S.E. (1989). Organization of the projection from the superficial to the deep layers of the hamster's superior colliculus as demonstrated by the anterograde transport of Phaseolus vulgaris leucoagglutinin. Journal of Comparative Neurology 283, 5470.CrossRefGoogle Scholar
Robson, J.A. & Hall, W.C. (1976). Projections from the superior colliculus to the dorsal lateral geniculate nucleus of the grey squirrel (Sciurus carolinensis). Brain Research 113, 379385.CrossRefGoogle Scholar
Robson, J.A. & Hall, W.C. (1977). The organization of the pulvinar in the grey squirrel (Sciurus carolinensis) I. cytoarchitecture and connections. Journal of Comparative Neurology 173, 355388.CrossRefGoogle ScholarPubMed
Sachs, G.M. & Schneider, G.E. (1984). The morphology of optic tract axons arborizing in the superior colliculus of the hamster. Journal of Comparative Neurology 230, 155167.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert monkey. Journal of Neurophysiology 34, 920937.CrossRefGoogle Scholar
Schiller, P.H. & Stryker, M. (1972). Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 35, 915924.CrossRefGoogle ScholarPubMed
Schiller, P.H., Stryker, M., Cynader, M. & Berman, N. (1974). Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. Journal of Neurophysiology 37, 181194.CrossRefGoogle ScholarPubMed
Schneider, G.E. & Jhaveri, S.R. (1974). Neuroanatomical correlates of spared or altered function after brain lesions in the newborn hamster. In Plasticity and Recovery of Function in the Central Nervous System, ed. Stein, D.G., Rosen, J.J. & Butters, N., pp. 65109. New York: Academic Press.Google Scholar
Sterling, P. (1971). Receptive fields and synaptic organization of the superficial gray layer of the cat superior colliculus. Vision Research 3, 309328.CrossRefGoogle Scholar
Sugita, S., Otani, K., Tokunaga, A. & Terasawa, K. (1983). Laminar origin of the tecto-thalamic projections in the albino rat. Neuroscience Letters 43, 143147.CrossRefGoogle ScholarPubMed
Tigges, J., Bos, J. & Tigges, M. (1977). An autoradiographic investigation of the subcortical visual system in chimpanzee. Journal of Comparative Neurology 172, 367380.CrossRefGoogle ScholarPubMed
Tigges, J. & Tigges, M. (1981). Distribution of retinofugal and corti-cofugal axon terminals in the superior colliculus of squirrel monkey. Investigative Ophthalmology and Visual Science 20, 149158.Google ScholarPubMed
Victorov, I.V. (1968). Neuronal structure of corpora quadrigemina in the cat. Arkhivy Anatomii, Gistologii i Embriologii 54, 4555.Google Scholar
Weber, J.T., Martin, G.F., Behan, M., Huerta, M.F. & Harting, J.K. (1979). The precise origin of the tectospinal pathway in three common laboratory animals: A study using the horseradish peroxidase method. Neuroscience Letters 11, 121127.CrossRefGoogle ScholarPubMed
Wiener, S.I. (1986). Laminar distribution and patchiness of cytochrome oxidase in mouse superior colliculus. Journal of Comparative Neurology 244, 137148.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Goldberg, M.F. (1972). Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements. Journal of Neurophysiology 35, 575586.CrossRefGoogle Scholar
Yamamoto, C. (1972). Activation of hippocampal neurons by mossy fiber stimulation in thin brain sections in vitro. Experimental Brain Research 14, 423435.CrossRefGoogle ScholarPubMed