Hostname: page-component-5c6d5d7d68-ckgrl Total loading time: 0 Render date: 2024-08-16T18:58:38.636Z Has data issue: false hasContentIssue false

Depth perception and cortical physiology in normal and innate microstrabismic cats

Published online by Cambridge University Press:  02 June 2009

C. Distler
Affiliation:
Lehrstuhl für Allgemeine Zoologie und Neurobiologie, Ruhr-Universitat Bochum, Bochum, Federal Republic of Germany
K.-P. Hoffmann
Affiliation:
Lehrstuhl für Allgemeine Zoologie und Neurobiologie, Ruhr-Universitat Bochum, Bochum, Federal Republic of Germany

Abstract

Evidence is presented that innate microstrabismus and abnormal cortical visual receptive-field properties can occur also in cats without any apparent involvement of the Siamese or albino genetic abnormalities in their visual system. A possible cause for microstrabismus in these cats may be sought in an abnormally large horizontal distance between blind spot and area centralis indicated by a temporal displacement of the most central receptive fields on both retinae.

Depth perception was found to be impaired in cats with innate microstrabismus. Behavioral measurements using a Y-maze revealed in four such cats that the performance in recognizing the nearer of two random-dot patterns did not improve when they were allowed to use both eyes instead of only one. The ability of microstrabismic cats to perceive depth under binocular viewing conditions only corresponded to the monocular performance of five normal cats.

Electrophysiological recordings were performed in the visual cortex (areas 17 and 18) of four awake cats, two normal, and two innate microstrabismic animals. Ocular dominance and orientation tuning of single neurons in area 17 and 18 were analyzed quantitatively.

The percentage of neurons in area 17 and 18 which could be activated through either eye was significantly reduced to 49.7% in the microstrabismic animals when compared to the normal cats (74.8%). “True binocular cells,” which can only be activated by simultaneous stimulation of both eyes, were significantly less frequent (1.6%) in microstrabismic cats than in normal animals (10.4%). However, subthreshold binocular interactions were identical in both groups of animals. In the strabismic animals, long-term binocular stimulation of monocular neurons did not give a clear indication of alternating use of one or the other eye.

The range of stimulus orientations leading to discharge rates above 50% of the maximal response, i.e. the half-width of the orientation tuning curves, was the same in the two groups of cats. However, orientation sensitivity, i.e. the alternation in discharge rate per degree change in stimulus orientation, was higher in cortical cells of normal cats than in those of microstrabismic cats.

In normal and microstrabismic cats, no clear sign of an “oblique effect,” i.e. the preference of cortical neurons for vertical and horizontal orientations compared to oblique orientations, could be found neither in the incidence of cells with horizontal or vertical preferred orientation nor in the sharpness of orientation tuning and sensitivity of these neurons.

In summary, the receptive-field properties reported here for awake innate microstrabismic cats are similar to those reported in the literature for anesthetized cats with varying degrees of albinism and for cats with artificial symmetrical strabismus surgically induced by sectioning the equivalent extraocular muscles in both eyes. Our innate microstrabismic cats may provide, however, an animal model for investigating the etiology of one form of naturally occurring strabismus.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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

Barlow, H.B., Blakemore, C. & Pettigrew, J.D. (1967). The neural mechanism of binocular depth discrimination. Journal of Physiology 193, 327342.CrossRefGoogle ScholarPubMed
Bennett, M.J., Smith, E.L., III, Harwerth, R.S. & Crawford, M.L.J. (1980). Ocular dominance, eye alignment, and visual acuity in kittens reared with an optically induced squint. Brain Research 193, 3345.CrossRefGoogle ScholarPubMed
Berman, N. & Murphy, H. (1982). The critical period for alteration in cortical binocularity resulting from divergent and convergent strabismus. Developmental Brain Research 2, 181202.CrossRefGoogle Scholar
Bisti, S. & Maffel, L. (1979). Binocular interaction in bilateral strabismic kittens. Brain Research 170, 359361.CrossRefGoogle ScholarPubMed
Blake, R. & Hirsch, H.V.B. (1975). Deficits in binocular depth perception in cats after alternating monocular deprivation. Science 190, 11141116.CrossRefGoogle ScholarPubMed
Campebell, F.W., Cleland, B.G., Cooper, G.F. & Enroth-Cugell, C. (1968). The angular selectivity of visual cortical cells to moving gratings. Journal of Physiology 198, 237250.CrossRefGoogle Scholar
Chino, Y.M., Shansky, M.S. & Pizzi, W.J. (1980). Receptive-field properties of simple and complex striate neurons in Siamese cats. Journal of Comparative Neurology 190, 6386.CrossRefGoogle ScholarPubMed
Chino, Y.M., Shansky, M.S., Jankowski, W.L. & Banser, F.A. (1983). Effects of rearing kittens with convergent strabismus on development of receptive-field properties in striate cortex neurons. Journal of Neurophysiology 50, 265286.CrossRefGoogle ScholarPubMed
Cooper, M.L. & Pettigrew, J.D. (1979 a). The decussation of the retinothalamic pathway in the cat, with a note on the major meridians of the cat's eye. Journal of Comparative Neurology 187, 285312.CrossRefGoogle ScholarPubMed
Cooper, M.L. & Pettigrew, J.D. (1979 b). The retinothalamic pathways in Siamese cats. Journal of Comparative Neurology 187, 313348.CrossRefGoogle ScholarPubMed
Creel, D., Hendrickson, A.E. & Leventhal, A.G. (1982). Retinal projections in tyrosinase-negative albino cats. The Journal of Neuroscience 2, 907911.CrossRefGoogle ScholarPubMed
Cynader, M., Gardner, J.C. & Mustari, M. (1984). Effects of neonatally induced strabismus on binocular responses in cat area 18. Experimental Brain Research 53, 384399.CrossRefGoogle ScholarPubMed
Distler, C. & Hoffmann, K.-P. (1989). The pupillary light reflex in normal and innate microstrabismic cats, 1: Behavior and receptive- field analysis in the nucleus praetectalis olivaris. Visual Neuroscience 3, 127138.CrossRefGoogle Scholar
Duke-Elder, S. & Wybar, K. (1973). Ocular motility and strabismus. In System of Opthalmology, Vol. VI, London: Kimpton.Google Scholar
Evinger, C. & Fuchs, A.F. (1978). Saccadic, smooth pursuit, and optokinetic eye movements of the trained cat. Journal of Physiology 285, 209229.CrossRefGoogle ScholarPubMed
Freeman, R.D. & Robson, J.G. (1982). A new approach to the study of binocular interaction in visual cortex: normal and monocularly deprived cats. Experimental Brain Research 48, 296300.CrossRefGoogle Scholar
Freeman, R.D. & Tsumoto, T. (1983). An electrophysiological comparison of convergent and divergent strabismus in the cat: electrical and visual activation of single cortical cells. Journal of Neurophysiology 49, 238253.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969). An abnormal retinogeniculate projection in Siamese cats. Brain Research 14, 739741.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1974). Visual pathways in albinos. Scientific American 230, 4454.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Kaas, J.H. (1973). Genetic abnormality of the visual pathways in a “white” tiger. Science 180, 12871289.CrossRefGoogle Scholar
Guillery, R.W., Hickey, T.L. & Spear, P.D. (1981). Do blue-eyed white cats have normal or abnormal retinofugal pathways? Investigative Ophthalmology and Visual Science 21, 2733.Google ScholarPubMed
Hammond, P. (1979). Stimulus dependence of ocular dominance of complex cells in area 17 of the feline visual cortex. Experimental Brain Research 35, 583589.CrossRefGoogle ScholarPubMed
Hammod, P. & Andrews, D.P. (1978). Orientation tuning of cells in area 17 and 18 of the cat's visual cortex. Experimental Brain Research 31, 341351.Google Scholar
Hegglund, P. & Albus, K. (1978). Orientation selectivity of single cells in striate cortex of cat: the shape of orientation tuning curves. Vision Research 18, 10671071.CrossRefGoogle Scholar
Henry, G.H., Dreher, B. & Bishop, P.O. (1974). Orientation specificity of cells in cat striate cortex. Journal of Neurophysiology 37, 13941409.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. & Cynader, M. (1977). Functional aspects of plasticity in the visual system of adult cats after early monocular deprivation. Philosophical Transactions of the Royal Society (London) 278, 411424.Google ScholarPubMed
Hoffmann, K-P. & Schoppmann, A. (1984). Shortage of binocular cells in area 17 of visual cortex in cats with congenital strabismus. Experimental Brain Research 55, 470482. Hoffmann, K.-P. & Markner, C. (In preparation). Optokinetic nystagmus in cats with congenital microstrabismus.CrossRefGoogle ScholarPubMed
Horn, A.K.E. & Hoffmann, K.-P. (1987). Combined GABA immunocytochemistry and TMB-HRP histochemistry of pretectal nuclei projecting to the inferior olive in rats, cats, and monkeys. Brain Research 409, 133138.CrossRefGoogle Scholar
Howard, H.J. (1919). A test of the judgement of distance. American Journal of Ophthalmology 2, 656.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1965). Binocular interaction in striate cortex of kittens reared with artificial squint. Journal of Neurophysiology 28, 10411059.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1971). Aberrant visual projections in the Siamese cat. Journal of Physiology 218, 3362.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1973). A reexamination of stereoscopic mechanisms in area 17 of the cat. Journal of Physiology 232, 2930P.Google ScholarPubMed
Joshua, D.E. & Bishop, P.O. (1970). Binocular single vision and depth discrimination. Receptive-field disparities for central and peripheral vision and binocular interaction on peripheral single units in cat striate cortex. Experimental Brain Research 10, 389416.CrossRefGoogle ScholarPubMed
Kalil, R.E., Spear, P.D. & Langsetmo, A. (1984). Response properties of striate cortex neurons in cats raised with divergent or convergent strabismus. Journal of Neurophysiology 52, 514537.CrossRefGoogle ScholarPubMed
Kaye, M., Mitchell, D.E. & Cynader, M. (1981). Selective loss of binocular depth perception after ablation of cat visual cortex. Nature 293, 6062.CrossRefGoogle ScholarPubMed
Kaye, M., Mitchell, D.E. & Cynader, M. (1982). Depth perception, eye alignment, and cortical ocular dominance of dark-reared cats. Developmental Brain Research 2, 3753.CrossRefGoogle Scholar
Kennedy, H. & Orban, G.A. (1979). Preferences for horizontal or vertical orientation in cat visual cortical neurons. Journal of Physiology 296, 6162.Google ScholarPubMed
Lehmkuhle, S.W. & Fox, R. (1975). Effect of binocular rivalry suppression on the motion aftereffect. Vision Research 15, 855859.CrossRefGoogle ScholarPubMed
Levelt, W.J.M. (1967). Note on the distribution of dominance times in binocular rivalry. British Journal of Psychology 58, 143145.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Vitek, D.J. & Creel, D.J. (1985). Abnormal visual pathways in normally pigmented cats that are heterozygous for albinism. Science 229, 13951397.CrossRefGoogle ScholarPubMed
Macy, A., Ohzawa, I. & Freeman, R.D. (1982). A quantitative study of the classification and stability of ocular dominance in the cat's visual cortex. Experimental Brain Research 48, 401408.CrossRefGoogle ScholarPubMed
Mesulam, M.M. (1978). Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualization of neuronal afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106117.CrossRefGoogle Scholar
Mitchell, D.E., Kaye, M. & Timney, B. (1979). Assessment of depth perception in cats. Perception 8, 389396.CrossRefGoogle ScholarPubMed
Mower, G.D., Burchfiel, J.L. & Duffy, F.H. (1982). Animal models of strabismic amblyopia: physiological studies of visual cortex and the lateral geniculate nucleus. Developmental Brain Research 5, 311327.CrossRefGoogle Scholar
Mueller, T. J. & Blake, R. (1989). A fresh look at the temporal dynamics of binocular rivalry. Biological Cybernetics 61, 223232.CrossRefGoogle Scholar
Noda, H., Freeman, R.B., Gies, B. & Creutzfeldt, O.D. (1971 a). Neuronal responses in the visual cortex of awake cats to stationary and moving targets. Experimental Brain Research 12, 389405.CrossRefGoogle Scholar
Noda, H., Creutzfeldt, O.D. & Freeman, R.B. (1971 b). Binocular interaction in the visual cortex of awake cats. Experimental Brain Research 12, 406421.CrossRefGoogle Scholar
Packwood, J. & Gordon, B. (1975). Stereopsis in normal domestic cat, Siamese cat, and cat raised with alternating monocular occlusion. Journal of Neurophysiology 38, 14851499.CrossRefGoogle Scholar
Pettigrew, J.D. & Dreher, B. (1987). Parallel processing of binocular disparity in the cat's retinogeniculocortical pathways. Proceedings of the Royal Society B (London) 232, 297324.Google ScholarPubMed
Pettigrew, J.D., Nikara, T. & Bishop, P.O. (1968 a). Binocular interaction on single units in cat striate cortex: simultaneous stimulation by single moving slit with receptive fields in correspondence. Experimental Brain Research 6, 391410.Google ScholarPubMed
Pettigrew, J.D., Nikara, T. & Bishop, P.O. (1968 b). Responses to moving slits by single units in cat striate cortex. Experimental Brain Research 6, 373390.Google ScholarPubMed
Schoppmann, A. & Hoffmann, K.-P. (1985). The development of eye alignment in normal and naturally microstrabismic kittens. Investigative Ophthalmology and Visual Science 26, 350358.Google ScholarPubMed
Shatz, C.J. (1977). A comparison of visual pathways in Boston and Midwestern Siamese cats. Journal of Comparative Neurology 171, 205228.CrossRefGoogle ScholarPubMed
Singer, W., Rauschecker, J. & von Gruenau, M. (1979 a). Squint affects striate cortex cells encoding horizontal image movements. Brain Research 170, 182186.CrossRefGoogle ScholarPubMed
Singer, W., von, Gruenau M. & Rauschecker, J. (1979 b). Requirements for the disruption of binocularity in the visual cortex of strabismic kittens. Brain Research 171, 536540.CrossRefGoogle ScholarPubMed
Singer, W., von, Gruenau M. & Rauschecker, J. (1980). Functional amblyopia in kittens with unilateral exotropia, I: Electrophysiological assessment. Experimental Brain Research 40, 294304.CrossRefGoogle ScholarPubMed
Skottun, B.C. & Freeman, R.D. (1984). Stimulus specificity of binocular cells in the cat's visual cortex: ocular dominance and the matching of left and right eyes. Experimental Brain Research 56, 206216.CrossRefGoogle ScholarPubMed
Timney, B. (1984). Monocular deprivation and binocular depth perception in kittens. In Development of Visual Pathways in Mammals ed. Stone, J., Dreher, B., & Rapaport, D., pp. 405423, New York: A.R. Liss Inc.Google Scholar
Van Sluyters, R.C. & Levitt, F.B. (1980). Experimental strabismus in the kitten. Journal of Neurophysiology 43, 686699.CrossRefGoogle ScholarPubMed
Vogels, R., Orban, G.A. & Vandenbussche, E. (1984). Meridional variations in orientation discrimination in normal and amblyopic vision. Investigative Ophthalmology and Visual Science 25, 720728.Google ScholarPubMed
Von Gruenau, M.W. (1982). Comparison of the effects of induced strabismus on binocularity in area 17 and the LS area in the cat. Brain Research 246, 325329.CrossRefGoogle Scholar
Von Gruenau, M.W. & Rauschecker, J.P. (1983). Natural strabismus in nonSiamese cats: lack of binocularity in the striate cortex. Experimental Brain Research 52, 307310.CrossRefGoogle Scholar
Yinon, U., Auerbach, E., Blank, M. & Friesenhausen, J. (1975). The ocular dominance of cortical neurons in cats developed with divergent and convergent squint. Vision Research 15, 12511256.CrossRefGoogle ScholarPubMed