Abstract
The neurophysiological consequences of artificial strabismus in cats and monkeys have been studied for 30 years. However, until very recently no clear picture has emerged of neural deficits that might account for the powerful interocular suppression that strabismic humans experience, nor for the severe amblyopia that is often associated with convergent strabismus. Here we review the effects of squint on the integrative capacities of the primary visual cortex and propose a hypothesis about the relationship between suppression and amblyopia. Most neurons in the visual cortex of normal cats and monkeys can be excited through either eye and show strong facilitation during binocular stimulation with contours of similar orientation in the two eyes. But in strabismic animals, cortical neurons tend to fall into two populations of monocularly excitable cells and exhibit suppressive binocular interactions that share key properties with perceptual suppression in strabismic humans. Such interocular suppression, if prolonged and asymmetric (with input from the squinting eye habitually suppressed by that from the fixating eye), might lead to neural defects in the representation of the deviating eye and hence to amblyopia.
Similar content being viewed by others
Article PDF
References
Graham PA . The epidemiology of strabismus. Br J Ophthalmol 1974; 58: 224–31.
Duke-Elder S, Wybar KC . Ocular motility and strabismus. In: Duke-Elder S, editor. System of ophthalmology. London: Henry Kimpton, 1973.
von Noorden GK . Binocular vision and ocular motility: theory and management of strabismus. St Louis: CV Mosby, 1990.
Mitchell DE . Animal models of human strabismic amblyopia: some observations concerning the interpretation of the effects of surgically and optically induced strabismus in cats and monkeys. In: Shinkman PG, editor. Advances in neural and behavioural development. Norwood, NJ: Ablex Publishing, 1988: 209–69.
von Grünau MW . Binocular summation and the binocularity of cat visual cortex. Vision Res 1979; 19: 813–6.
Crawford MLJ, Smith EL III, Harwerth RS, von Noorden GK . Stereoblind monkeys have few binocular neurons. Invest Ophthalmol Vis Sci 1984; 25: 779–81.
von Noorden GK, Dowling JE . Experimental amblyopia in monkeys. II. Behavioural studies in strabismic amblyopia. Arch Ophthalmol 1970; 84: 215–20.
Iked H, Jacobson SG . Nasal field loss in cats reared with convergent squint: behavioural studies. J Physiol (Lond) 1977; 270: 367–81.
von Grünau MW, Singer W . Functional amblyopia in kittens with unilateral exotropia. II. Correspondence between behavioural and electrophysiological assessment. Exp Brain Res 1980; 40: 305–10.
Roelfsema PR, König P, Engel AK, Sireteanu R, Singer W . Reduced synchronization in the visual cortex of cats with strabismic amblyopia. Eur J Neurosci 1994; 6: 1645–55.
Hubel DH, Wiesel TN . Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 1965; 28: 1041–59.
Blakemore C . The conditions required for the maintenance of binocularity in the kitten's visual cortex. J Physiol (Lond) 1976; 261: 423–44.
Van Sluyters RC, Levitt FB . Experimental strabismus in the kitten. J Neurophysiol 1980; 43: 686–99.
Singer W, von Grünau MW, Rauschecker JP . Functional amblyopia in kittens with unilateral exotropia. I. Electrophysiological assessment. Exp Brain Res 1980; 40: 294–304.
Crewther DP, Crewther SG . Neural site of strabismic amblyopia in cats: spatial frequency deficit in primary cortical neurons. Exp Brain Res 1990; 79: 615–22.
Sengpiel F, Blakemore C, Kind PC, Harrad R . Interocular suppression in the visual cortex of strabismic cats. J Neurosci 1994; 14: 6855–71.
Baker FH, Grigg P, von Noorden GK . Effects of visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in the normal animal. Brain Res 1974; 66: 185–208.
Crawford MLJ, von Noorden GK . The effects of short-term experimental strabismus on the visual system in Macaca mulatta. Invest Ophthalmol Vis Sci 1979; 18: 496–505.
Blake R, Cormack RH . Psychophysical evidence for a monocular visual cortex in stereoblind humans. Science 1979; 203: 274–5.
Lema S, Blake R . Binocular summation in normal and stereoblind humans. Vision Res 1977; 17: 691–5.
Levi DM, Harwerth RS, Smith EL III. Humans deprived of normal binocular vision have binocular interactions tuned to size and orientation. Science 1979; 206: 852–4.
Jacobs DS, Blakemore C . Factors limiting the postnatal development of visual acuity in the monkey. Vision Res 1988; 28: 947–58.
Levi DM, Klein SA . Vernier acuity, crowding and amblyopia. Vision Res 1985; 25: 979–91.
Hess RF, Field DJ, Watt RJ . The puzzle of amblyopia. In: Blakemore C, editor. Vision: coding and efficiency. Cambridge: Cambridge University Press, 1990: 267–80.
Blakemore C, Vital-Durand F . Different neural origins for ‘blur’ amblyopia and strabismic amblyopia. Ophthalmic Physiol Opt 1992; 12: 83.
Wiesel TN, Hubel DH . Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 1963; 26: 1003–17.
Blakemore C, Garey LJ, Vital-Durand F . The physiological effects of monocular deprivation and their reversal in the monkey's visual cortex. J Physiol (Lond) 1978; 283: 223–62.
Eggers HM, Blakemore C . Physiological basis of anisometropic amblyopia. Science 1978; 201: 264–7.
Movshon JA, Eggers HM, Gizzi MS, Hendrickson AE, Kiorpes L, Boothe RG . Effects of early unilateral blur on the macaque's visual system. III. Physiological observations. J Neurosci 1987; 7: 1340–51.
Mower GD, Burchfield JL, Duffy FH . Animal models of strabismic amblyopia: physiological studies of visual cortex and the lateral geniculate nucleus. Dev Brain Res 1982; 5: 311–27.
Sireteanu R, Singer W, Fronius M, Greuel JM, Best J, Fiorentini A, et al. Eye alignment and cortical binocularity in strabismic kittens: a comparison between tenotomy and recession. Vis Neurosci 1993; 10: 541–9.
Blakemore C . Maturation of mechanisms for efficient spatial vision. In: Blakemore C, editor. Vision: coding and efficiency. Cambridge: Cambridge University Press, 1990: 254–66.
Blakemore C, Eggers HM . Animal models for human visual development. In: Cool SJ, Smith EL III, editors. Frontiers in visual science. New York: Springer, 1978: 651–9.
Sengpiel F . Mechanisms of binocular integration in the mammalian primary visual cortex. DPhil thesis, University of Oxford, 1994.
Movshon JA, Kiorpes L . Biological limits on visual developments in primates. In: Simons K, editor. Early visual development, normal and abnormal. Oxford: Oxford University Press, 1993; 296–305.
Ikeda H, Wright MJ . Properties of LGN cells in kittens reared with convergent squint: a neurophysiological demonstration of amblyopia. Exp Brain Res 1976; 25: 63–77.
Ikeda H, Tremain KE . Amblyopia occurs in retinal ganglion cells in cats reared with convergent squint without alternating fixation. Exp Brain Res 1979; 35: 559–82.
Cleland BG, Crewther DP, Crewther GS, Mitchell DE . Normality of spatial resolution of retinal ganglion cells in cats with strabismic amblyopia. J Physiol (Lond) 1982; 326: 235–49.
Crewther SG, Crewther DP . Neural site of strabismic amblyopia in cats: X-cell acuities in the LGN. Exp Brain Res 1988; 72: 503–9.
Hess RF, Campbell FW, Greenhalgh T . On the nature of the neural abnormality in human amblyopia: neural aberrations and neural sensitivity loss. Pflugers Arch 1978; 377: 201–7.
Levi DM, Klein S . Hyperacuity and amblyopia. Nature 1982; 298: 268–70.
Swindale NV, Mitchell DE . Comparison of receptive field properties of neurons in area 17 of normal and bilaterally amblyopic cats. Exp Brain Res 1994; 99: 399–410.
Chino YM, Shansky MS, Jankowski WL, Banser FA . Effects of rearing kittens with convergent strabismus on development of receptive-field properties in striate cortex neurons. J Neurophysiol 1983; 50: 265–86.
Yinon U, Auerbach E, Blank M, Friesenhausen J . The ocular dominance of cortical neurons in cats developed with divergent and convergent squint. Vision Res 1975; 15: 1251–6.
Berman N, Murphy EH . The critical period for alteration in cortical binocularity resulting from divergent and convergent strabismus. Dev Brain Res 1982; 2: 181–202.
Freeman RD, Tsumoto T . An electrophysiological comparison of convergent and divergent strabismus in the cat: electrical and visual activation of single cortical cells. J Neurophysiol 1983; 49: 238–53.
Kalil RE, Spear PD, Langsetmo A . Response properties of striate cortex neurons in cats raised with divergent or convergent strabismus. J Neurophysiol 1984; 52: 514–37.
Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, et al. Coherent oscillations: a mechanism of feature linking in the visual cortex? Biol Cybern 1988; 60: 121–30.
Gray CM, König P, Engel AK, Singer W . Oscillatory responses in cat visual cortex exhibit inter-columnar synchronizations which reflects global stimulus properties. Nature 1989; 338: 334–7.
Engel AK, König P, Gray CM, Singer W . Stimulus dependent neuronal oscillations in cat visual cortex: intercolumnar interaction as determined by cross-correlation analysis. Eur J Neurosci 1990; 2: 588–606.
Singer W . Search for coherence: a basic principle of cortical self-organization. Neurosci Concepts 1990; 1: 1–26.
König P, Engel AK, Löwel S, Singer W . Squint affects synchronization of oscillatory responses in cat visual system. Eur J Neurosci 1993; 5: 501–8.
Löwel S, Singer W . Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 1992; 255: 209–12.
Nelson JI . Binocular vision: disparity detection and anomalous correspondence. In: Edwards K, Llewellyn R, editors. Optometry. London: Butterworth, 1988: 217–37.
Schor CM . Binocular sensory disorders. In: Regan D, editor. Vision and visual dysfunction, vol 9: Binocular vision. London: Macmillan Press, 1991: 179–223.
Travers T . Suppression of vision in squint and its association with retinal correspondence and amblyopia. Br J Ophthalmol 1938; 22: 577–604.
Sireteanu R, Fronius M . Naso-temporal asymmetries in human amblyopia: consequence of long-term interocular suppression. Vision Res 1981; 21: 1055–63.
Sireteanu R . Binocular vision in strabismic humans with alternating fixation. Vision Res 1982; 22: 889–96.
Sireteanu R . Human amblyopia: consequence of chronic interocular suppression. Human Neurobiol 1982; l: 31–3.
Barlow HB, Blakemore C, Pettigrew JD . The neural mechanism of binocular depth perception. J Physiol (Lond) 1967; 193: 327–42.
Pettigrew JD, Nikara T, Bishop PO . Binocular interaction on single units in cat striate cortex: simultaneous stimulation by single moving slit with receptive fields in correspondence. Exp Brain Res 1968; 6: 391–410.
Ohzawa I, Freeman RD . The binocular organization of simple cells in the cat's visual cortex. J Neurophysiol 1986; 56: 221–42.
Ohzawa I, Freeman RD . The binocular organization of complex cells in the cat's visual cortex. J Neurophysiol 1986; 56: 243–59.
Sengpiel F, Blakemore C . Interocular control of neuronal responsiveness in cat visual cortex. Nature 1994; 368: 847–50.
Sengpiel F, Blakemore C, Harrad R . Interocular suppression in the primary visual cortex: a possible neural basis of binocular rivalry. Vision Res 1995; 35: 179–95.
Leopold DA, Logothetis NK . Cell activity reflects monkey's perception during binocular rivalry. Invest Ophthalmol Vis Sci 1995; 36: S813.
Holopigian K, Blake R, Greenwald MJ . Clinical suppression and amblyopia. Invest Ophthalmol Vis Sci 1988; 29: 444–51.
Livingstone MS, Hubel DH . Segregation of form, colour, movement and depth: anatomy, physiology and perception. Science 1988; 240: 740–9.
Jampolsky A . Characteristics of suppression in strabismus. Arch Ophthalmol 1955; 54: 683–96.
Thiele A, Bremmer F, Ilg UJ, Hoffmann K-P . Response properties of neurons in cortical areas V1, MT and MST of a monkey with late-onset strabismus. Eur J Neurosci Suppl 1992; 5: 263.
Sengpiel F, Kind P, Harrad RA, Blakemore C . Effects of induced strabismus and of dark-rearing on interocular interactions in cat area 17. In: Eisner N, Heisenberg M, editor. Gene — brain — behaviour (Proceedings of the 21st Göttingen Neurobiology Conference). Stuttgart: Thieme, 1993: 433.
Chino YM, Smith EL III, Yoshida K, Cheng H, Hamamoto J . Binocular interactions in striate cortical neurons of cats reared with discordant visual inputs. J Neurosci 1994; 14: 5050–67.
Freeman RD, Ohzawa I . Monocularly deprived cats: binocular tests of cortical cells reveal functional connections from the deprived eye. J Neurosci 1988; 8: 2491–506.
Rauschecker JP . Mechanisms of visual plasticity: Hebb synapses, NMDA receptors and beyond. Physiol Rev 1991; 71: 587–615.
Sengpiel F, Freeman TCB, Blakemore C . Interocular suppression in cat striate cortex is not orientation selective. Neuroreport 1995; 6: 2235–9.
Ts'o D, Gilbert CD, Wiesel TN . Relationships between horizontal connections and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci 1986; 6: 1160–70.
Schwarz C, Bolz J . Functional specificity of a long-range horizontal connection in cat visual cortex: a cross-correlation study. J Neurosci 1991; 11: 2995–3007.
Albus K, Wahle P . The topography of tangential inhibitory connections in the postnatally developing and mature striate cortex of the cat. Eur J Neurosci 1994; 6: 779–92.
Kisvárday ZF, Eysel UT . Functional and structural topography of horizontal inhibitory connections in cat visual cortex. Eur J Neurosci 1993; 5: 1558–72.
Kisvárday ZF, Kim D-S, Eysel UT, Bonhoeffer T . Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex. Eur J Neurosci 1994; 6: 1619–32.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sengpiel, F., Blakemore, C. The neural basis of suppression and amblyopia in strabismus. Eye 10, 250–258 (1996). https://doi.org/10.1038/eye.1996.54
Issue Date:
DOI: https://doi.org/10.1038/eye.1996.54
Keywords
This article is cited by
-
Management of amblyopia in pediatric patients: Current insights
Eye (2022)
-
A covered eye fails to follow an object moving in depth
Scientific Reports (2021)
-
Abnormal intra-network architecture in extra-striate cortices in amblyopia: a resting state fMRI study
Eye and Vision (2019)
-
Kindlicher Strabismus in Deutschland: Prävalenz und Risikogruppen
Bundesgesundheitsblatt - Gesundheitsforschung - Gesundheitsschutz (2017)
-
Mechanisms of recovery of visual function in adult amblyopia through a tailored action video game
Scientific Reports (2015)