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Interlaminar connections of the superior colliculus in the tree shrew. III: The optic layer

Published online by Cambridge University Press:  02 June 2009

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

These experiments were designed to test the idea that the optic layer in the tree shrew, Tupaia belongeri, is functionally distinct and provides a link between the visuosensory superficial and the premotor intermediate layers of the superior colliculus. First, cells in the optic layer were intracellularly labeled with biocytin in living brain slices. Compared to cells in the adjacent lower part of the superficial gray layer, which have apical dendrites that ascend toward the tectal surface, optic layer cells have dendritic fields that are restricted for the most part to the optic layer itself. The differences in dendritic-field location imply that superficial gray and optic layer cells have different patterns of input. The axons of optic layer cells terminate densely within the optic layer and, in addition, project in a horizontally restricted fashion to the overlying superficial gray and subjacent intermediate gray layers. This pattern also is different from the predominantly descending interlaminar projections of lower superficial gray layer cells. Next cells in the intermediate gray layer were labeled in order to examine the relationships between optic layer cells and these subjacent neurons that project from the superior colliculus to oculomotor centers of the brain stem Neurons in the upper part of the intermediate gray layer send apical dendrites into the optic layer and therefore can receive signals from the superficial gray layer either directly, from descending axons of lower superficial gray layer cells, or indirectly, through intervening optic layer cells. In contrast, lower intermediate gray layer cells have more radiate dendritic fields that are restricted to the intermediate gray layer. Thus, these lower cells must depend on descending projections from optic or upper intermediate gray layer cells for signals from the superficial gray layer. Together, these results support the idea that the optic layer is a distinct lamina that provides a link between the superficial and intermediate gray layers. They also are consistent with the traditional view that descending intracollicular projections play a role in the selection of visual targets for saccades.

Keywords

MidbrainSensorimotorVisuomotorEye movements
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 4 , July 1997 , pp. 647 - 661
Copyright
Copyright © Cambridge University Press 1997

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References

Abramson, B.P. & Chalupa, L.M. (1988). Multiple pathways from the superior colliculus to the extrageniculate visual thalamus of the cat. Journal of Comparative Neurology 271, 397–418.CrossRefGoogle Scholar
Adams, J.C. (1981). Heavy metal intensification of DAB-based reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Aghajanian, G.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, 331–338.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, 1–11.CrossRefGoogle ScholarPubMed
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, 591–604.CrossRefGoogle Scholar
Behan, M. & Appell, P.P. (1992). Intrinsic circuitry in the cat superior colliculus: Projections from the superficial layers. Journal of Comnarative Neurology 315, 230–243.CrossRefGoogle ScholarPubMed
Berson, D.M. (1985). Cat lateral suprasylvian cortex: Y-cell inputs and corticotectal projection. Journal of Neurophysiology 53, 544–555CrossRefGoogle ScholarPubMed
Berson, D.M. (1988). Retinal and cortical inputs to cat superior colliculus: Composition, convergence, and laminar specificity. In Progress in Brain Research, Vol. 75, ed. Hicks, T.P. & Benedek, G., pp. 17–26. Amsterdam: Elsevier Science Publishers.Google 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, 253–292.CrossRefGoogle ScholarPubMed
Chalupa, L.M., Williams, R.W. & Hughes, M.J. (1983). Visual response properties in the tecto-recipient zone of the cat's lateral posteriorpulvinar complex: A comparison with the superior colliculus. Journal of Neuroscience 3, 2587–2596.CrossRefGoogle Scholar
Chevalier, G. & Deniau, J.M. (1990). Disinhibition as a basic process in the expression of striatal functions. Trends in Neuroscience 13, 277–280.CrossRefGoogle ScholarPubMed
Clemo, H.R. & Stein, B.E. (1986). Effects of cooling somatosensory cortex on response properties of tactile cells in the superior colliculus. Journal of Neurophysiology 55, 1352–1368.CrossRefGoogle ScholarPubMed
Deng, S-Y., Goldberg, M.E., Segraves, M.A., Ungerleider, L.G. & Mishkin, M. (1986). The effect of unilateral ablation of the frontal eye fields on saccadic performance in the monkey. In Adaptive Processes in Visual and Oculomotor Systems, ed. Keller, E.L. & Zee, D.S., pp. 201–208. Oxford: Pergamon.Google Scholar
Fischer, B. & Boch, R. (1981). Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkey. Experimental Brain Research 44, 129–137.CrossRefGoogle Scholar
Glimcher, P.W. & Sparks, D.L. (1992). Movement selection in advance of action in the superior colliculus. Nature 355, 542–545.CrossRefGoogle ScholarPubMed
Glimcher, P.W. & Sparks, D.L. (1993). Effects of low-frequency stimulation of the superior colliculus on spontaneous and visually guided saccades. Journal of Neurophysiology 69, 953–964.CrossRefGoogle ScholarPubMed
Goldberg, M.E. & Wurtz, R.H. (1972 a). Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. Journal of Neurophysiology 35, 542–559.CrossRefGoogle ScholarPubMed
Goldberg, M.E. & Wurtz, R.H. (1972 b). Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. Journal of Neurophysiology 35, 560–574.CrossRefGoogle ScholarPubMed
Goldman, P.S. & Nauta, W.J.H. (1976). Autoradiographic demonstration of a projection from prefrontal association cortex to the superior colliculus in the rhesus monkey. Brain Research 116, 145–149.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, 133–151.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, 557–580.CrossRefGoogle ScholarPubMed
Grantyn, A. & Grantyn, R. (1982). Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbospinal tract. Experimental Brain Research 46, 243–256.CrossRefGoogle ScholarPubMed
Grantyn, R. (1988). Gaze control through the superior colliculus: Structure and function. In Neuroanatomy of the Oculomotor System, ed. Büttner-Ennever, J.A., pp. 273–333. Amsterdam: Elsevier Science Publishers.Google Scholar
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, 172–176.CrossRefGoogle Scholar
Graybiel, A.M. (1978). A stereometric pattern of distribution of acetylthiocholinesterase in the deep layers of the superior colliculus. Nature 272, 539–541.CrossRefGoogle ScholarPubMed
Groh, J.M. & Sparks, D.L. (1996 a). Saccades to somatosensory targets. II. Motor convergence in primate superior colliculus. Journal of Neurophysiology 75, 428–438.CrossRefGoogle ScholarPubMed
Groh, J.M. & Sparks, D.L. (1996 b). Saccades to somatosensory targets. III. Eye-position-dependent somatosensory activity in primate superior colliculus. Journal of Neurophysiology 75, 439–453.CrossRefGoogle ScholarPubMed
Haenny, P.E., Maunsell, J.H.R. & Schiller, P.H. (1988). State dependent activity in monkey visual cortex. II. Retinal and cxtrarctinal factors in V4. Experimental Brain Research 69, 245–259.CrossRefGoogle ScholarPubMed
Hall, W.C., Fitzpatrick, D., Klatt, L.L. & Raczkowski, D. (1989). Cholinergic innervation of the superior colliculus in the cat. Journal of Comparative Neurology 287, 495–514.CrossRefGoogle ScholarPubMed
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, 213–223.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, 379–414.CrossRefGoogle ScholarPubMed
Hikosaka, O. & Wurtz, R.H. (1985). Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in the monkey substantia nigra pars reticulata. Journal of Neurophysiology 53, 292–308.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, 409–424.CrossRefGoogle Scholar
Illing, R.-B. (1990). Choline acetyltransferase-like immunorcactivity in the superior colliculus and its relation to the pattern of acetylcholinesterase staining. Journal of Comparative Neurology 296, 32–46.CrossRefGoogle Scholar
Itoh, K., Conley, M. & Diamond, I.T. (1981). Different distributions of large and small ganglion cells in the cat after HRP injections of single layers of the lateral geniculate body and the superior colliculus. Brain Research 207, 147–152.CrossRefGoogle ScholarPubMed
Jay, M.F. & Sparks, D.L. (1987 a). Sensorimotor integration in the primate superior colliculus. I. Motor convergence. Journal of Neurophysiology 57, 22–34.CrossRefGoogle ScholarPubMed
Jay, M.F. & Sparks, D.L. (1987 b). Sensorimotor integration in the primate supcrior colliculus. II. Coordinates of auditory signals. Journal of Neurophysiology 57, 35–55.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, 1–16.CrossRefGoogle Scholar
Keating, E.G. (1991). Frontal eye field lesions impair predictive and visually-guided pursuit eye movements. Experimental Brain Research 86, 311–323.CrossRefGoogle ScholarPubMed
Keller, E.L. (1979). Colliculoreticular organization in the oculomotor system. In Reflex Control of Posture and Movement, Progress in Brain Research, ed. Granit, R. & Pompeiano, O., pp. 725–734. Amsterdam: Elsevier.CrossRefGoogle Scholar
Keller, E.L. & Edelman, J.A. (1994). Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey. Journal of Neurophysiology 72, 2754–2770.CrossRefGoogle ScholarPubMed
Kuypers, H.G.J.M. & Lawrence, D.G. (1967). Cortical projections to the red nucleus and the brain stem in the rhesus monkey. Brain Research 4, 151–188.CrossRefGoogle Scholar
Lee, P. & Hall, W.C. (1995). Interlaminar connections of the superior colliculus in the tree shrew. II. Projections from the superficial gray to the optic layer. Visual Neuroscience 12, 573–588.CrossRefGoogle Scholar
Leichnetz, G.R., Spencer, R.F., Hardy, S.G.P. & Astruc, J. (1981). The prefrontal corticotectal projection in the monkey; an anterograde and retrograde horseradish peroxidase study. Neuroscience 6, 1023–1041.CrossRefGoogle ScholarPubMed
Lynch, J.C., Graybiel, A.M. & Lobeck, L.J. (1985). The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. Journal of Comparative Neurology 235, 241–254.CrossRefGoogle ScholarPubMed
Ma, T.P., Graybiel, A.M. & Wurtz, R.H. (1991). Location of saccaderelated neurons in the macaque superior colliculus. Experimental Brain Research 85, 21–35.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, 357–376.CrossRefGoogle ScholarPubMed
May, P.J., Hall, W.C., Porter, J.D. & Sakai, S.T. (1993). The comparative anatomy of nigral and cerebellar control over tectally initiated orienting movements. In Role of the Cerebellum and Basal Ganglia in Voluntary Movement, ed. Mano, N., Hamada, I. & Delong, M.R., pp. 221–231. Amsterdam: Elsevier Science Publishers.Google Scholar
May, P.J. & Porter, J.D. (1992). The laminar distribution of macaque tectobulbar and tectospinal neurons. Visual Neuroscience 8, 257–276.CrossRefGoogle ScholarPubMed
Mays, L.E. & Sparks, D.L. (1980). Dissociation of visual and saccaderelated responses in superior colliculus neurons. Journal of Neurophysiology 43, 207–232.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1975). Visual receptive fields and their images in superior colliculus of the cat. Journal of Neurophysiology 38, 219–230.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. 223–248, Baltimore, Maryland: 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, 133–138.CrossRefGoogle Scholar
Meredith, M.A., Wallace, M.T. & Stein, B.E. (1992). Visual, auditory and somatosensory convergence in output neurons of the cat superior colliculus: Multisensory properties of the tecto-reticulo-spinal projection. Experimental Brain Research 88, 181–186.CrossRefGoogle ScholarPubMed
Mohler, C.W. & Wurtz, R.H. (1976). Organization of monkey superior colliculus: Intermediate layer cells discharging before eye movements. Journal of Neurophysiology 39, 722–744.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, 1384–1399.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, 1333–1351.CrossRefGoogle Scholar
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, 276–308.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, 232–262.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, 263–302.CrossRefGoogle ScholarPubMed
Motter, B.C. (1993). Focal attention produces spatially selective processing in visual cortical areas V1, V2 and V4 in the presence of competing stimuli. Journal of Neurophysiology 70, 909–919.CrossRefGoogle ScholarPubMed
Motter, B.C. (1994). Neural correlates of attentive selection for color or luminance in extrastriate area V4. Journal of Neuroscience 14, 2178–2189.CrossRefGoogle ScholarPubMed
Mower, G., Gibson, A. & Glickstein, M. (1979). Tectopontine pathway in the cat: Laminar distribution of cells of origin and visual properties of target cells in dorsolateral pontine nucleus. Journal of Neurophysiology 42, 1–15.CrossRefGoogle ScholarPubMed
Munoz, D.P. & Guitton, D. (1986). Presaccadic burst discharges of tecto-reticulo-spinal neurons in the alert head-free and -fixed cat. Brain Research 398, 185–190.CrossRefGoogle ScholarPubMed
Munoz, D.P. & Guitton, D. (1991). Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. Journal of Neurophysiology 66, 1624–1641.CrossRefGoogle Scholar
Munoz, D.P. & Wurtz, R.H. (1995). Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. Journal of Neurophysiology 73, 2313–2333.CrossRefGoogle ScholarPubMed
Naegele, J.R. & Katz, L.C. (1990). Cell surface molecules containing N-acetylgalactosamine are associated with basket cells and neurogliaform cells in cat visual cortex. Journal of Neuroscience 10, 540–557.CrossRefGoogle ScholarPubMed
Norden, J.J., Lin, C.S. & Kaas, J.H. (1978). Subcortical projections of the dorsomedial visual area (DM) of visual association cortex in the owl monkey, Aotus trivirgatus. Experimental Brain Research 32, 321–334.CrossRefGoogle ScholarPubMed
Robinson, D.L. & McClurkin, J.W. (1989). The visual superior colliculus and pulvinar. In The Neurobiology of Saccadic Eye Movements, ed. Wurtz, R.H. & Goldberg, M.F., pp. 337–360. Amsterdam: Elsevier Science Publishers.Google Scholar
Schall, J.D. (1995). Neural basis of saccade target selection. Reviews in Neuroscience 6, 63–85.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert monkey. Journal of Neurophysiology 34, 920–937.CrossRefGoogle Scholar
Schiller, P.H. & Stryker, M. (1972). Single unit recording and stimulation in superior colliculus of the alert monkey. Journal of Neurophysiology 35, 915–924.CrossRefGoogle Scholar
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, 181–194.CrossRefGoogle ScholarPubMed
Schlag-Rey, M., Schlag, J. & Dassonville, P. (1992). How the frontal eye field can impose a saccade goal on superior colliculus neurons. Journal of Neurophysiology 67, 1003–1005.CrossRefGoogle ScholarPubMed
Sparks, D.L. (1978). Functional properties of neurons in the monkey superior colliculus: Coupling of neuronal activity and saccade onset. Brain Research 156, 1–16.CrossRefGoogle ScholarPubMed
Sparks, D.L., Holland, R. & Guthrie, B.L. (1976). Size and distribution of movement fields in the monkey superior colliculus. Brain Research 113, 21–34.CrossRefGoogle ScholarPubMed
Stanton, G.B., Goldberg, M.E. & Bruce, C.J. (1988). Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. Journal of Comparative Neurology 271, 493–506.CrossRefGoogle ScholarPubMed
Stein, B.E., Magalhaes-Castro, B. & Kruger, L. (1976). Relationship between visual and tactile representations in cat superior colliculus. Journal of Neurophysiology 39, 401–419.CrossRefGoogle ScholarPubMed
Stein, B.E., Spencer, R.F. & Edwards, S.B. (1983). Corticotectal and corticothalamic efferent projections of SIV somatosensory cortex in cat. Journal of Neurophysiology 50, 896–909.CrossRefGoogle ScholarPubMed
Ungerleider, L.G., Desimone, R., Galkin, T.W. & Mishkin, M. (1984) Subcortical projections of area MT in the macaque. Journal of Comparative Neurology 223, 368–386.CrossRefGoogle ScholarPubMed
Van Gisbergen, J.A.M., Van Opstal, A.J. & Tax, A.A.M. (1987). Collicular ensemble coding of saccades based on vector summation. Neuroscience 21, 541–555.CrossRefGoogle ScholarPubMed
Walker, M.F., Fitzgibbon, E.J. & Goldberg, M.E. (1995). Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. Journal of Neurophysiology 73, 1988–2003.CrossRefGoogle ScholarPubMed
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, 121–127.CrossRefGoogle ScholarPubMed
Webster, M.J., Bachevalier, J. & Ungerleider, L.G. (1993). Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. Journal of Comparative Neurology 335, 73–91.CrossRefGoogle ScholarPubMed
Weliky, M., Kandler, K., Fitzpatrick, D. & Katz, L.C. (1995). Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns. Neuron 15, 541–552.CrossRefGoogle Scholar
Wickelgren, B.G. (1971). Superior colliculus: Some receptive field properties of bimodally responsive cells. Science 173, 69–72.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, 575–586.CrossRefGoogle Scholar
Wurtz, R.H. & Mohler, C.W. (1976 a). Organization of monkey superior colliculus: Enhanced visual response of superficial layer cells. Journal of Neurophysiology 39, 745–765.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Mohler, C.W. (1976 b). Enhancement of visual responses in monkey striate cortex and frontal eye fields. Journal of Neuronhysiology 39, 766–772.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Optican, L.M. (1994). Superior colliculus cell types and models of saccade generation. Current Opinion in Neurobiology 4 857–861.CrossRefGoogle ScholarPubMed