Summary
In two cats in which surgically induced, unilateral divergent strabismus had led to behaviourally determined amblyopia, a variety of electrophysiological parameters were determined in search of neuronal correlates of squint amblyopia. Tests that assess global neuronal excitability along the pathways from the two eyes to the visual cortex (areas 17 and 18) failed to reflect the functional inferiority of the squinting eye: retinographic responses and cortical evoked potentials elicited by Ganzfeld-stimulation and by stimulation of the optic nerves were identical for the two eyes. The ocular dominance distribution of neurons in area 17 showed the expected disruption of binocularity but failed to provide clear evidence for a functional inferiority of the squinting eye. At other levels of analysis, however, a clear difference between the two eyes was apparent:
-
1.
Responses to optimally aligned light stimuli tended to be more sluggish and the under-representation of neurons with vertically oriented receptive fields was more pronounced in neurons driven from the deviated eye than in cells dominated by the normal one.
-
2.
Interocular inhibition as assessed from electrically evoked potentials was found to be asymmetric; responses evoked from the amblyopic eye were suppressed more readily and over longer periods by conditioning shocks applied to the normal nerve than vice versa.
-
3.
Numerous abnormalities reflecting the functional inferiority of the squinting eye became apparent in cortical potentials evoked by phase reversal of gratings of variable spatial frequency and contrast. A laminar analysis of these field potentials suggests impaired transmission along the intracortical pathways which relay activity to supragranular layers as a major cause for abnormal responses from the squinting eye. It is concluded that squint amblyopia is associated with a variety of neuronal changes at various levels of the visual system, the present data providing evidence for alterations at the cortical level.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baker FH, Grigg P, Noorden GK von (1974) Effects of visual deprivation and strabismus on the response of neurones in the visual cortex of the monkey, including studies on the striate and prestriate cortex in the normal animal. Brain Res 66: 185–208
Burian HM, Lawwill T (1966) Electroretinographic studies in strabismic amblyopia. Am J Ophthalmol 61: 422–430
Crawford MLJ, Noorden GK von (1979) The effects of short-term experimental strabismus on the visual system in Macaca mulatta. Invest Ophthalmol Visual Sci 18: 496–505
Duke-Elder S (1973) System of ophthalmology, vol 6, Ocular motility and strabismus. Kimpton, London
Freeman JA, Nicholson C (1975) Experimental optimization of current source-density technique for anuran cerebellum. J Neurophysiol 38: 369–382
Freeman JA, Stone J (1969) A technique for current density analysis of field potentials and its application to the frog cerebellum. In: Llinas R (ed) Neurobiology of cerebellar evolution and development. American Medical Association, Chicago, pp 421–430
Gilbert CD (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex. J Physiol (Lond) 268: 391–421
Grünau M von (1978) Luminance dependence of strabismic amblyopia in kittens. J Physiol (Lond) 284: 118
Grünau M von, Singer W (1980) Functional amblyopia in kittens with unilateral exotropia. II. Correspondence between behavioural and electrophysiological assessment. Exp Brain Res 40: 305–310
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol (Lond) 160: 106–154
Hubel DH, Wiesel TN (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 28: 1041–1059
Ikeda H, Wright MJ (1976) Properties of LGN cells in kittens reared with convergent squint. A neurophysiological demonstration of amblyopia. Exp Brain Res 25: 63–77
Ikeda H, Tremain KE (1977) Different causes for amblyopia and loss of binocularity in squinting kittens. J Physiol (Lond) 269: 26–27
Ikeda H, Tremain KE (1979) Amblyopia occurs in retinal ganglion cells in cats reared with convergent squint without alternating fixation. Exp Brain Res 35: 559–582
Ikeda H, Tremain KE, Binon G (1978) Loss of spatial resolution of lateral geniculate nucleus neurones in kittens raised with convergent squint produced at different stages in development. Exp Brain Res 31: 207–220
Jacobson SG, Ikeda H (1979) Behavioural studies of spatial vision in cats reared with convergent squint. Is amblyopia due to arrest of development? Exp Brain Res 34: 11–26
Mitzdorf U, Singer W (1978) Prominent excitatory pathways in the cat visual cortex (A17 and A18). A current source density analysis of electrically evoked potentials. Exp Brain Res 33: 371–394
Mitzdorf U, Singer W (1980) Monocular activation of visual cortex (A17 and A18) in normal and monocularly deprived cats. J Physiol (Lond) (in press)
Nawratzki I, Auerbach E, Rowe H (1966) Amblyopia ex anopsia. The electrical response in retina and occipital cortex following photic stimulation of normal and amblyopic eyes. Am J Ophthalmol 61: 430–435
Nicholson C, Freeman JA (1975) Theory of current source-density analysis and determination of conductivity tensor for Anuran cerebellum. J Neurophysiol 38: 356–368
Rauschecker JP, Singer W (1979) Changes in the circuitry of the kitten's visual cortex are gated by postsynaptic activity. Nature 280: 58–60
Sanderson KJ, Bishop PO, Darian-Smith J (1971) The properties of the binocular receptive fields of lateral geniculate neurons. Exp Brain Res 13: 178–207
Sherman SM (1972) Development of interocular alignment in cats. Brain Res 37: 187–203
Singer W (1970) Inhibitory binocular interaction in the lateral geniculate body of the cat. Brain Res 18: 165–170
Singer W (1973) The effect of mesencephalic reticular stimulation on intracellular potentials of cat lateral geniculate neurons. Brain Res 61: 35–54
Singer W (1977) Effects of monocular deprivation on excitatory and inhibitory pathways in cat striate cortex. Exp Brain Res 30: 25–41
Singer W (1978) The effect of monocular deprivation on cat parastriate cortex. Asymmetry between crossed and uncrossed pathways. Brain Res 157: 351–355
Singer W (1979) Neuronal mechanisms in experience dependent modification of visual cortex function. In: Bloom F, Cuenod M, Kreutzberg G (eds) Development and chemical specificity of neurons. Progress in Brain Research, vol 51. Eisevier, Amsterdam, pp 457–477
Singer W, Bedworth N (1973) Inhibitory interaction between X and Y units in the cat lateral geniculate nucleus. Brain Res 49: 291–307
Singer W, Tretter F, Cynader M (1975) Organization of cat striate cortex. A correlation of receptive field properties with afferent and efferent connections. J Neurophysiol 38: 1080–1098
Singer W, Tretter F, Cynader M (1976) The effect of reticular stimulation on spontaneous and evoked activity in the cat visual cortex. Brain Res 102: 71–90
Singer W, Yinon W, Tretter F (1979a) Inverted monocular vision prevents ocular dominance shift in kittens and impairs the functional state of visual cortex in adult cats. Brain Res 164: 294–299
Singer W, Rauschecker J, Grünau M von (1979b) Squint affects striate cortex cells encoding horizontal image movements. Brain Res 170: 182–186
Singer W, Grünau M von, Rauschecker J (1979c) Requirements for the disruption of binocularity in the visual cortex of strabismic kittens. Brain Res 171: 536–540
Suzuki H, Takahashi M (1973) Distribution of binocular inhibitory interaction in the lateral geniculate nucleus of the cat. Tohoku J Exp Med 111: 393
Wiesel TN, Hubel DH (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26: 1003–1017
Yinon U, Auerbach E, Blank M, Friesenhausen J (1975) The ocular dominance of cortical neurones in cats developed with divergent and convergent squint. Vision Res 15: 1251–1256
Author information
Authors and Affiliations
Additional information
This work was partially supported by a grant from the Deutsche Forschungsgemeinschaft SFB 50 A.14
Rights and permissions
About this article
Cite this article
Singer, W., von Grünau, M. & Rauschecker, J. Functional amblyopia in kittens with unilateral exotropia. Exp Brain Res 40, 294–304 (1980). https://doi.org/10.1007/BF00237794
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00237794