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The Neural Basis of Suppression and Amblyopia in Strabismus

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The Neural Basis of Suppression and Amblyopia in Strabismus THE NEURAL BASIS OF SUPPRESSION AND AMBLYOPIA IN STRABISMUS FRANK SENGPIEL and COLIN BLAKEMORE Oxford SUMMARY with exotropia (divergent squint), possibly because The neurophysiological consequences of artificial stra­ of the higher prevalence of alternating fixation and/ bismus in cats and monkeys have been studied for 30 or, frequently, the later onset of deviation. Stereopsis years. However, until very recently no clear picture has is either absent or very deficient in all forms of emerged of neural deficits that might account for the strabismus, whether or not one eye is amblyopic. In powerful interocular suppression that strabismic addition, there are a variety of other deficits in humans experience, nor for the severe amblyopia that binocular visual function. 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 NEURAL SUBSTRATES OF AMBLYOPIA about the relationship between suppression and For 30 years, artificial (surgically or optically amblyopia. Most neurons in the visual cortex of normal induced) squint in cats and monkeys has served as cats and monkeys can be excited through either eye and an animal model of human strabismus.4 Just as in show strong facilitation during binocular stimulation humans, animals with strabismus have impaired with contours of similar orientation in the two eyes. But stereopsiss,6 and can become amblyopic in the in strabismic animals, cortical neurons tend to fall into deviating eye?-lO However, despite considerable two populations of monocularly excitable cells and efforts, neurophysiological studies have failed until exhibit suppressive binocular interactions that share very recently to reveal central deficits that might key properties with perceptual suppression in strabis­ account for either the severe acuity loss that often mic humans. Such interocular suppression, if prolonged occurs in the deviating eye of strabismic humans and and asymmetric (with input from the squinting eye animals or for some of the more subtle defects of habitually suppressed by that from the fixating eye), binocular function. Most investigators have simply might lead to neural defects in the representation of the studied the responses of individual cortical neurons deviating eye and hence to amblyopia. in the primary visual cortex (VI) to monocular stimulation: strabismus of early onset was found to Strabismus is one of the most frequent visual cause a breakdown of conventional 'binocularity'. disorders in human beings, with a childhood inci­ Most cells in the visual cortex of strabismic catsll-16 dence of about 6%.1 Various categories can be and monkeys6,1 7,18 can be driven through only one discerned clinically, depending on the age of onset, eye, either left or right, seldom through both, and the state of fixation, presumed aetiology, etc. (for slight variation in cortical ocular dominance across reviews see Duke-Elder and von Noorden3). the cortex seen in normal animals becomes trans­ Among them, esotropia, or convergent squint, is formed in sharply defined ocular dominance (OD) the commonest form, with a relative prevalence of columns. There is indirect evidence that this also about 67%.1 In the majority of cases, it is associated holds true for VI of strabismic humans.19 This loss of with unilateral fixation and amblyopia in the non­ 'binocular' neurons is assumed to underlie the fixating eye, i.e. a deficit in visual acuity, in the defects of binocular summation and stereopsis in absence of any recognisable ocular pathology, which strabismic animalss,6 and humans?O,21 persists even when refractive errors have been Visual acuity, as assessed with conventional corrected. There is a lower incidence of amblyopia optotypes, depends on both the detection and the localisation of variations of contrast in the retinal Correspondence to: Frank Sengpiel, University Laboratory of Physiology, Parks Road, Oxford OX1 3PT, UK. Fax: +44 (01865) image. For an emmetropic eye, visual acuity is 272 488. e-mail: [email protected]. normally determined by spatial sampling of the Eye (1996) 10,250-258 © 1996 Royal College of Ophthalmologists NEUROPHYSIOLOGY OF STRABISMUS 251 image in the eye. Indeed, for humans and monkeys, In earlier reports, Ikeda and her colleagues had acuity in the central fieldappears to be limited by the described much more dramatic reductions in neural mosaic of foveal cones.22 In principle, then, the acuity in strabismic cats, for cells of the lateral reduction in acuity that characterises amblyopia geniculate nucleus (LGN)36 and for retinal ganglion could be due to one or a combination of three cells?7 However, later studies established that different causes: (1) a decrease in the number of behavioural amblyopia can occur with no detectable sampling channels at some point in the retina or effects in the retina38 or the LGN?3,39 visual pathway, leading to undersampling of the Errors in the central representation of the relative image and hence an incomplete central representa­ positions of parts of the image may be the cause of tion of the visual stimulus; (2) coarsening of the several perceptual problems experienced in ambly­ 'grain' of spatial sampling, e.g. as a result of opia, most obviously the spatial distortion of the convergence of signals on to central neurons, leading visual scene40 but also impaired vernier acuiti3,41 to a decrease in neural 'acuity'; or (3) some kind of and the spatial interference of contours, or 'crowd­ 'scrambling' of the central representation, causing ing', that many amblyopic humans complain of. positional uncertainty in that representation.23-25 There is some evidence of 'scrambling' of receptive In the case of deprivation amblyopia and anisome­ fields in VI of cats with deprivation amblyopia.42 tropic amblyopia, there is a partial 'disconnection' of Unusually large43 and scattered receptive fields44 the affected eye from the primary visual cortex. have also been reported for neurons in VI of Whereas in normal cats and monkeys the vast strabismic cats. However, the vast majority of studies majority of cortical neurons respond to stimulation suggest that the monocular receptive field properties through either eye, in animals that have been reared differ little from those in normal cats14,16,30,33,45-47 with one eye closed or defocused, the proportion of except, perhaps, in the representation of the extreme cortical neurons responding through the affected eye nasal visual field of the deviating eye in esotropic is much reducedp,26--29 Thus, in these kinds of animals.47 amblyopia the image might be undersampled at the More recent studies have focused on the possible level of the cortex (depending on the degree of effects of strabismus on the integrative capacities of oversampling, if any, in the normal animal). On the the visual cortex, and it is in this area where other hand, the evidence for neural undersampling in substantial anomalies have recently been described. strabismus is much less consistent. Some reports of In the normal cortex, neurons with similar stimulus cortical cells in strabismic monkeys17,18 and (less preferences tend to fire impulses synchronously strikingly) cats30,31 have described a bias in the when visually stimulated simultaneously,48,49 even if ocular dominance of cortical neurons, fewer respond­ their receptive fields do not overlap.50 This synchro­ ing through the deviating than the normal eye. nisation, which normally occurs whether the two cells However, most studies,6,1l-14,16 even in cats and are activated with stimuli falling in the same eye or in monkeys with demonstrated behavioural ambly­ different eyes, has been hypothesised to play an opia,15,25 have reported roughly equal numbers of important role in 'binding' the activity of the various neurons responding through the squinting and the feature-detecting neurons that respond to a particu­ non-squinting eye. lar global contour, surface or object into a coherent Similarly, there is much clearer evidence for a representation, and to distinguish that representation deficit in neural 'acuity' in deprivation and anisome­ from those for other, nearby contours, surfaces or tropic amblyopia than in strabismus?5 After early objects (for a review, see Singe�l). Now, in VI of occlusion or defocus of one eye, the minority of cells strabismic cats, neurons dominated by one eye tend in the cortex that still respond through that eye tend not to synchronise their firing with cells dominated to have diffuse, insensitive receptive fields and hence by the other eye.1O,52 This loss of synchronisation have poor spatial resolution and sensitivity to between neurons in neighbouring OD columns contrast.28,29,32 On the other hand, several studies correlates with the fact that the long-range intrinsic on strabismic catslO,33,34 and monkeys,25 even with connectivity which is such a striking feature of proven amblyopia, have revealed that cortical cells normal VI is specifically reduced between OD responding through the deviating eye have, at best, columns for different eyes in strabismic cats.53 spatial resolving power and contrast sensitivity Moreover, in esotropic cats with behaviourally indistinguishable from the best neural acuity of verified amblyopia, neurons dominated by the cells driven through the normal eye. However, in normal eye exhibit stronger synchronisation of cats with litrabismic amblyopia, Crewther and responses with each other than do those dominated Crewther15
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