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Visual detection deficits following inactivation of the superior colliculus in the cat

Published online by Cambridge University Press:  30 March 2004

MARNIE C. FITZMAURICE ,
VIVIAN M. CIARAMITARO ,
LARRY A. PALMER  and
ALAN C. ROSENQUIST
MARNIE C. FITZMAURICE
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
VIVIAN M. CIARAMITARO
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
LARRY A. PALMER
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
ALAN C. ROSENQUIST
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
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Abstract

Lesion or inactivation of the superior colliculus (SC) of the cat results in an animal that fails to orient toward peripheral visual stimuli which normally evoke a brisk, reflexive orienting response. A failure to orient toward a visual stimulus could be the result of a sensory impairment (a failure to detect the visual stimulus) or a motor impairment (an inability to generate the orienting response). Either mechanism could explain the deficit observed during SC inactivation since neurons in the SC can carry visual sensory signals as well as motor commands involved in the generation of head and eye movements. We investigated the effects of SC inactivation in the cat in two ways. First, we tested cats in a visual detection task that required the animals to press a central, stationary foot pedal to indicate detection of a peripheral visual stimulus. Such a motor response does not involve any components of the orienting response and is unlikely to depend on SC motor commands. A deficit in this task would indicate that the SC plays an important role in the detection of visual targets even in a task that does not require visual orienting. Second, to further investigate the visual orienting deficit observed during SC inactivation and to make direct comparisons between detection and orienting performance, we tested cats in a standard perimetry paradigm. Performance in both tasks was tested following focal inactivation of the SC with microinjections of muscimol at various depths and rostral/caudal locations throughout the SC. Our results reveal a dramatic deficit in both the visual detection task and the visual orienting task following inactivation of the SC with muscimol.

Keywords

Superior colliculusVisual detectionVisual orientingMuscimol
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 6 , November 2003 , pp. 687 - 701
Copyright
© 2003 Cambridge University Press

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References

REFERENCES

Albano, J.E., Mishkin, M., Westbrook, L.E., & Wurtz, R.H. (1982). Visuomotor deficits following ablation of monkey superior colliculus. Journal of Neurophysiology 48, 338–351.Google Scholar
Altman, J. & Carpenter, M.B. (1961). Fiber projections of the superior colliculus in the cat. Journal of Comparative Neurology 116, 157–178.Google Scholar
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, 261–268.Google Scholar
Behan, M. & Appell, P.P. (1992). Intrinsic circuitry in the cat superior colliculus: Projections from the superficial layers. Journal of Comparative Neurology 315, 230–243.Google Scholar
Berman, A.L. (1968). The Brainstem of the Cat: A Cytoarchitectonic Atlas with Stereotaxic Coordinates. Madison, Wisconsin: University of Wisconsin Press.
Berman, N. & Cynader, M. (1972). Comparison of receptive-field organization of the superior colliculus in siamese and normal cats. Journal of Physiology 224, 363–389.Google Scholar
Berson, D.M. & Graybiel, A.M. (1978). Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent and efferent connections. Brain Research 147, 139–148.Google Scholar
Berson, D.M. & McIlwain, J.T. (1982). Retinal Y-cell activation of deep-layer cells in the superior colliculus of cat. Journal of Neurophysiology 47, 700–714.Google Scholar
Butter, C.M., Weinstein, C., Bender, D., & Gross, C.G. (1978). Localization and detection of visual stimuli following superior colliculus in rhesus monkeys. Brain Research 156, 33–49.Google Scholar
Casagrande, V.A., Harting, J.K., Hall, W.C., & Diamond, I.T. (1972). Superior colliculus of the tree shrew: A structural and functional subdivision into superficial and deep layers. Science 177, 444–447.Google Scholar
Doya, K. (2000). Complementary roles of the basal ganglia and cerebellum in learning and motor control. Current Opinions in Neurobiology 10, 732–739.Google Scholar
Feldon, S., Feldon, P., & Kruger, L. (1970). Topography of the retinal projection upon the superior colliculus of the cat. Vision Research 10, 135–143.Google Scholar
Freedman, E.G. & Sparks, D.L. (1997). Activity of cells in the deeper layers of the superior colliculus of the rhesus monkey: Evidence for a gaze displacement command. Journal of Neurophysiology 78, 1669–1690.Google Scholar
Fuchs, A.F. & Robinson, D.A. (1966). A method for measuring horizontal and vertical eye movement chronically in the monkey. Journal of Applied Physiology 21, 1068–1070.Google Scholar
Gordon, B. (1973). Receptive fields in deep layers of cat superior colliculus. Journal of Neurophysiology 36, 157–178.Google Scholar
Graham, J. (1977). An autoradiographic study of the efferent connections of the superior colliculus in the cat. Journal of Comparative Neurology 173, 629–654.Google Scholar
Graybiel, A.M., Aosaki, T., Flaherty, A.W., & Kimura, M. (1994). The basal ganglia and adaptive motor control. Science 265, 1826–1831.Google Scholar
Harting, J.K., Huerta, M.F., Hashikawa, T., & Lieshout, D.P.V. (1991). Projection of the mamallian superior colliculus upon the dorsolateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species. Journal of Comparative Neurology 304, 275–306.Google Scholar
Harting, J.K., Updyke, B.V., & Lieshout, D.P.V. (2001). The visual-oculomotor striatum of the cat:functional relationship to the superior colliculus. Experimental Brain Research 136, 138–142.Google Scholar
Hikosaka, O. & Wurtz, R.H. (1983). Effects on eye movements of a GABA agonist and antagonist injected into monkey superior colliculus. Brain Research 272, 368–372.Google Scholar
Hikosaka, O. & Wurtz, R.H. (1985a). Modification of saccadic eye movements by GABA-related substances. I. Effects of muscimol and bicuculline in monkey superior colliculus. Journal of Neurophysiology 53, 266–291.Google Scholar
Hikosaka, O. & Wurtz, R.H. (1985b). Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. Journal of Neurophysiology 53, 292–308.Google Scholar
Hikosaka, O., Takikawa, Y., & Kawagoe, R. (2000). Role of the basal ganglia in the control of purposive saccadic eye movements. Physiological Reviews 80, 953–978.Google Scholar
Huerta, M. & Harting, J.K. (1984). Connectional organization of the superior colliculus. Trends in Neurosciences, 286–289.Google Scholar
Keating, E.G. & Gooley, S.G. (1988). Saccadic disorders caused by cooling the superior colliculus or the frontal eye field, or from combined lesions of both structures. Brain Research 438, 247–255.Google Scholar
Kurtz, D. & Butter, C.M. (1980). Impairments in visual discrimination performance and gaze shifts in monkeys with superior colliculus lesions. Brain Research 196, 109–124.Google Scholar
LaFlamme, D.P. (1993). Body condition scoring and weight maintenance. Proceedings of the North American Veterinary Conference, 291–292.
Latto, R. (1977). The effects of bilateral frontal eye-field, posterior parietal or superior collicular lesions on brightness thresholds in the rhesus monkey. Neuropsychologia 15, 507–516.Google Scholar
Lee, C., Rohrer, W.H., & Sparks, D.L. (1988). Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357–360.Google Scholar
Lomber, S.G., Payne, B.R., & Cornwall, P. (2001). Role of the superior colliculus in analyses of space: Superficial and intermediate layer contributions to visual orienting, auditory orienting and visuospatial discriminations during unilateral and bilateral deactivations. Journal of Comparative Neurology 441, 44–57.Google Scholar
Mays, L.E. & Sparks, D.L. (1980). Dissociation of visual and saccade-related responses in superior colliculus neurons. Journal of Neurophysiology 43, 207–232.Google Scholar
Mize, R.R. & White, D.A. (1989). Muscimol labels neurons in both the superficial and deep layers of cat superior colliculus. Neuroscience Letters 104, 31–37.Google Scholar
Moody, D.B. (1970). Reaction time as an index of sensory function. In Animal Psychophysics, ed. Stebbins, W.C., pp. 277–302. New York: Appleton-Century-Crofts.
Mower, G., Gibson, A., Robinson, F., Stein, J., & Glickstein, M. (1980). Visual pontocerebellar projections in the cat. Journal of Neurophysiology 43, 355–366.Google Scholar
Munoz, D.P. & Guitton, D. (1991a). Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. I. Identification, localization and effects of behavior on sensory responses. Journal of Neuroscience 66, 1605–1623.Google Scholar
Munoz, D.P. & Guitton, D. (1991b). Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. Journal of Neuroscience 66, 1624–1641.Google Scholar
Overton, P. & Dean, P. (1988). Detection of visual stimuli after lesions of the superior colliculus in the rat; deficit not confined to the far periphery. Behavioral Brain Research 31, 1–15.Google Scholar
Payne, B.R., Lomber, S.G., Geeraerts, S., & Gucht, E.V. (1996). Reversible visual hemineglect. Proceedings of the National Academy of Sciences of the U.S.A. 93, 290–294.Google Scholar
Peck, C., Schlag-Rey, M., & Schlag, J. (1980). Visuo-oculomotor properties of cells in the superior colliculus of the alert cat. Journal of Comparative Neurology 194, 97–116.Google Scholar
Peck, C.K. (1989). Visual responses of neurons in cat superior colliculus in relation to fixation of targets. Journal of Physiology 414, 301–315.Google Scholar
Peck, C.K. & Baro, J.A. (1997). Discharge patterns of neurons in the rostral superior colliculus of the cat: Activity related to fixation of visual and auditory targets. Experimental Brain Research 113, 291–302.Google Scholar
Reinoso-Suarez, F. (1961). Topographisher hirnatlas der katze fur experimental-physiologische untersuchungen. Darmstadt: E Merck.
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 34, 920–936.Google Scholar
Schultz, W., Tremblay, L., & Hollerman, J.R. (1998). Reward prediction in primate basal ganglia and frontal cortex. Neuropharmacology 37, 421–429.Google Scholar
Sparks, D.L. & Nelson, J.S. (1987). Sensory and motor maps in the mammalian SC. Trends in Neurosciences 10, 312–317.Google Scholar
Sparks, D.L. & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. In The Neurobiology of Saccadic Eye Movements, ed. Wurtz, R.H. & Goldberg, M.E., pp. 213–255. Elsevier Science Publishers BV.
Sprague, J.M. & Meikle, T.H. (1965). The role of the superior colliculus in visually guided behavior. Experimental Neurology 11, 115–146.Google Scholar
Stein, B.E. & Meredith, M.A. (1991). Functional organization of the superior colliculus. In The Neural Basis of Visual Function, ed. Levinthal, A.G., pp. 85–110. London: Macmillan Press.
Stein, B.E. & Meredith, M.A. (1993). The Merging of the Senses. Cambridge, Massachusetts: MIT Press.
Stein, J.F. & Glickstein, M. (1992). Role of the cerebellum in visual guidance of movement. Physiological Reviews 72, 967–1017.Google Scholar
Stuphorn, V., Hoffman, K.P., & Miller, L.E. (1999). Correlation of primate superior colliculus and reticular formation discharge with proximal limb muscle activity. Journal of Neurophysiology 81, 1978–1982.Google Scholar
Torrealba, F., Partlow, G.D., & Guillery, R.W. (1981). Organization of the projection from the superior colliculus to the dorsolateral geniculate nucleus of the cat. Neuroscience 6, 1341–1360.Google Scholar
Tunkl, J.E. & Berkley, M.A. (1977). The role of the superior colliculus in vision: Visual form discrimination in cats with superior colliculus ablations. Journal of Comparative Neurology 176, 575–587.Google Scholar
Vanduffel, W., Vandenbussche, E., Singer, W., & Orban, G.A. (1997). A metabolic mapping study of orientation discrimination and detection tasks in the cat. European Journal of Neuroscience 9, 1314–1328.Google Scholar
Vievard, A., Fabre-Thorpe, M., & Buser, P. (1986). Role of the extra-geniculate pathway in visual guidance I. Effects of lesioning the superior colliculus in the cat. Experimental Brain Research 62, 587–595.Google Scholar
Werner, W. (1993). Neurons in the primate superior colliculus are active before and during arm movements to visual targets. European Journal of Neuroscience 5, 335–340.Google Scholar
Werner, W., Hoffmann, K.P., & Dannenberg, S. (1997). Anatomical distribution of arm-movement-related neurons in the primate superior colliculus and underlying reticular formation in comparison with visual and saccadic cells. Experimental Brain Research 115, 206–216.Google Scholar
Wurtz, R.H. & Albano, J.E. (1980). Visual-motor function of the primate superior colliculus. Annual Review of Neuroscience 3, 189–226.Google Scholar
Wurtz, R.H. & Goldberg, M.E. (1972). Activity of superior colliculus in behaving monkeys. III. Cells discharging before eye movements. Journal of Neurophysiology 35, 575–586.Google Scholar