Neural mechanisms underlying amblyopia

Current Opinion in Neurobiology

Volumn 9, Issue 4, 1999, Pages 480-486

  Kiorpes, Lynne ^a   McKee, Suzanne P ^b  

^a NEW YORK UNIVERSITY   (United States)

^b SMITH KETTLEWELL EYE RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMBLYOPIA; MONKEY; NERVE CONDUCTION; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; VISUAL CORTEX; VISUAL IMPAIRMENT;

EID: 0033179334     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)80072-5     Document Type: Article

References (54)

1. 1. von Noorden GK: Burien-von Noorden's Binocular Vision and Ocular Motility. St Louis: Mosby; 1980.
2. 2. Daw NW: Critical periods and amblyopia. Arch Ophthalmol 1998, 116:502-505. This carefully written paper is a clear and thoughtful discussion of critical periods in vision and their relationship to visual development. Daw reminds us that 'the' critical period is, in fact, different for different visual functions and has essentially three (non-exclusive) stages: one that is synonymous with the period of visual development, a second one during which deprivation can cause a loss of vision, and a third one during which treatment can effect improvement in vision.
3. 3. Daw NW: Visual Development. New York: Plenum;1995.
4. 4. Kiorpes L, Carlson MR, Alfi D: Development of visual acuity in experimentally strabismic monkeys. Clin Vis Sci 1989, 4:95-106.
5. 5. Levi DM, Carkeet A: Amblyopia: a consequence of abnormal visual development. In Early Visual Development: Normal and Abnormal. Edited by Simons K. New York: Oxford University Press; 1993:391-408.
6. 6. Kiorpes L, Kiper DC, Movshon JA: Contrast sensitivity and Vernier acuity in amblyopic monkeys. Vision Res 1993, 33:2301-2311.
7. 7. Kiorpes L, Movshon JA: Amblyopia: a developmental disorder of the central visual pathways. Cold Spring Harb Symp Quant Biol 1996, 61:39-48.
8. 8. Harwerth RS, Smith EL, Boltz RL, Crawford MLJ, von Noorden GK: Behavioral studies on the effect of abnormal early visual experience: spatial modulation sensitivity. Vision Res 1983, 4:1501-1510.
9. 9. Smith EL, Harwerth RS, Crawford MLJ: Spatial contrast sensitivity deficits in monkeys produced by optically induced anisometropia. Invest Ophthalmol Vis Sci 1985, 26:330-342.
10. 10. McKee, SP: Binocular functioning and visual acuity in amblyopia. Maternal and Child Health Bureau; Department of Health and Human Services. Conference proceedings Vision Screening in the Preschool Child, Sept 10-11, 1998.
11. 11. Simons K: Stereoscopic neurontropy and the origins of amblyopia and strabismus. In Early Visual Development: Normal and Abnormal. Edited by Simons K. New York: Oxford University Press; 1993:409-453.
12. 12. Sengpiel F, Blakemore C: The neural basis of suppression and amblyopia in strabismus. Eye 1996, 10:250-258.
13. 13. 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 of striate and prestriate cortex in the normal animal. Brain Res 1994, 66:185-208.
14. 14. Wiesel TN: Postnatal development of the visual cortex and the influence of environment Nature 1982, 299:583-591.
15. 15. Hendrickson AE, Movshon JA, Eggers HM, Gizzi MS, Boothe RG, Kiorpes L: Effects of early unilateral blur on the macaque's visual system. II. Anatomical observations. J Neurosci 1987, 7:1327-1339.
16. 16. Delint P, Weissenbruch C, Berendschot TTJM, Van Nooren D: Photoreceptor function in unilateral amblyopia. Vision Res 1998, 38:613-617.
17. 17. Lempert P, Porter L: Dysversion of the optic disc and axial length measurements in a presumed amblyopic population. J Am Assoc Pediatric Ophthalmol Strabismus 1998, 2:207-213.
18. 18. 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, 7:1340-1351.
19. 19. Sasaki Y, Cheng H, Smith EL, Chino Y: Effects of early discordant binocular vision on the postnatal development of parvocellular neurons in the monkey lateral geniculate nucleus. Exp Brain Res 1998, 118:341-351.
20. 20. Blakemore C, Vital-Durand F: Effects of visual deprivation on the development of the monkey's lateral geniculate nucleus. J Physiol (Lond) 1986, 380:493-511.
21. 21. Levitt JB, Movshon JA, Sherman SM, Spear PD: Effects of monocular deprivation on macaque LGN. Invest Ophthalmol Vis Sci 1989, 30:S296.
22. 22. Sloper JJ: Competition and cooperation in visual development. Eye 1993, 7:319-331.
23. 23. Eggers HM, Blakemore C: Physiological basis of anisometropic amblyopia. Science 1978, 201:264-267.
24. 24. Crewther DP, Crewther SG: Neural site of strabismic amblyopia in cats: spatial frequency deficit in primary cortical neurons. Exp Brain Res 1990, 79:615-622.
25. 25. Kiorpes L, Kiper DC, O'Keefe LP, Cavanaugh JR, Movshon JA: Neuronal correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia. J Neurosci 1998,18:6411 -6424. This study represents the first comprehensive study of spatial properties of V1 neurons in primates with behaviorally documented strabismic amblyopia. The report includes experimentally anisometropic (lens-reared) as well as strabismic monkeys. The study confirms previous reports showing reduced binocularity in amblyopic monkeys and shows that for severe amblyopes, there is a shift in the balance of representation of the two eyes away from the amblyopic eye. The primary finding is that there is a shift in the spatial frequency response properties of neurons driven by the amblyopic eye to lower spatial frequencies. On balance then, the population of neurons driven by the amblyopic eye has larger receptive fields and, in some cases, lower contrast sensitivity than the neurons driven by the fellow eye. The neurophysiological losses correlate well with behaviorally measured losses in visual function, but are somewhat smaller. It is likely that these losses are the initial neural correlate of amblyopia in the central visual pathways, but there are additional deficits at higher levels of the system.
26. 26. Smith EL, Chino YM, Ni J, Cheng H, Crawford MLJ, Harwerth RS: Residual binocular interactions in the striate cortex of monkeys reared with abnormal binocular vision. J Neurophysiol 1997, 78:1353-1362.
27. 27. Lowell S, Singer W: Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 1992, 255:209-212.
28. 28. Tyschen L, Burkhalter A: Neuroanatomic abnormalities of primary visual cortex in macaque monkeys with infantile esotropia: preliminary results. J Ped Ophthalmol Strab 1995, 32:323-328.
29. 29. Roelfsema PR, Konig P, Engel AK, Sireteanu R, Singer W: Reduced synchronization in the visual cortex of cats with strabismic amblyopia. Eur J Neurosci 1994, 6:1645-1655.
30. 30. Mitchell DE: The long-term effectiveness of different regimens of occlusion on recovery from early monocular deprivation in kittens. Philos Trans R Soc Lond [Biol] 1991, 333:51-79.
31. 31. Chino YM, Shansky MS, Jankowski WL, Banser FA: Effects of rearing kittens with convergent strabismus on the development of receptive field properties in striate cortex neurons. J Neurophysiol 1983, 50:265-286.
32. 32. Brody CD: Slow covariations in neuronal resting potentials can lead to artefactually fast cross-correlations in their spike trains. J Neurophysiol 1998, 80:3345-3351.
33. 33. Levi DM, Klein SA: Vernier acuity, crowding, and amblyopia. Vision Res 1985, 25:979-991.
34. 34. Levi DM, Klein SA: Sampling in spatial vision. Nature 1986, 320:360-362.
35. 35. Levi DM, Klein SA: Limitations on position coding imposed by undersampling and univariance. Vision Res 1996, 36:2111-2120.
36. 36. Hess RF, Campbell FW, Greenhalgh T: On the nature of the neural abnormality in human amblyopia; neural aberrations and neural sensitivity loss. Pflug Arch 1978, 377:201-207.
37. 37. Hess RF, Field DJ, Watt RJ: The puzzle of amblyopia. In Vision Coding and Efficiency. Edited by Blakemore C. Cambridge: Cambridge University Press; 1990:267-280.
38. 38. Hess RF, Wang Y-Z, Demanins R, Wilkinson F, Wilson HW: A deficit in strabismic amblyopia for global shape detection. Vision Res 1999, 39:901-914. This is a unique approach to the question of the nature of the strabismic amblyopic deficit. Normal and strabismic amblyopic observers were asked to detect deformations from circularity in a large band-limited stimulus. Strabismic amblyopes were more impaired on this shape discrimination task compared to normals. Modeling of the results showed that both neural disarray and undersampling could account for the results. The authors favored the disarray hypothesis because the undersampling would need to be scale invariant to completely capture the strabismic deficit.
39. 39. Wilson HR: Model of peripheral and amblyopic hyperacuity. Vision Res 1991, 21:967-982.
40. 40. Hess RF, Field DJ: Is the spatial deficit in strabismic amblyopia due to loss of cells or an uncalibrated disarray of cells? Vision Res 1994, 24:3397-3406.
41. 41. Maloney LT, Ahumada AJ: Learning by assertion: two methods for calibrating a linear visual system. Neural Computation 1989, 1:392-401.
42. 42. Watt RJ, Hess RF: Spatial information and uncertainty in anisometropic amblyopia. Vision Res 1987, 27:661-674.
43. 43. Wang H, Levi DM, Klein SA: Spatial uncertainty and sampling efficiency in amblyopic position acuity. Vision Res 1998, 38:1239-1251. This study was designed to test the idea that positional jitter was the primary limitation in strabismic amblyopia and evaluate the extent to which strabismic and anisometropic amblyopia can be characterized by reduced sampling efficiency. They found an increased tolerance for positional jitter in both types of amblyopes compared to normals; strabismic amblyopes had particularly poor sampling efficiency, suggesting that they have fewer filters available for encoding the stimulus.
44. 44. Levi DM, Klein SA, Sharma V: Position jitter and undersampling in pattern perception. Vision Res 1999, 39:445-465. This study attempts to distinguish topographic jitter and undersampling as explanations for the strabismic amblyopic visual deficit. The authors used a pattern-recognition task (Figure 3e-g) to compare the performance of normal observers, using foveal and peripheral viewing, with that of strabismic amblyopes. (The extensive literature on the comparison between amblyopic vision and normal peripheral vision is not addressed in this review; the interested reader can follow the topic up from this reference.) The ratio of detection threshold to identification threshold is similar in all cases; if topographic jitter was a consistent feature of strabismic amblyopia, identification thresholds should be elevated. The study also found that normal and strabismic observers had similar tolerance for positional jitter of the elements within the pattern, but that strabismics needed more elements for pattern identification. This suggests that the stimulus is underrepresented, rather than jumbled, in the strabismic visual system, which supports the undersampling hypothesis.
45. 45. Kiorpes L, Movshon JA: The effect of blur and jitter on Vernier acuity in normal and amblyopic macaque monkeys. Perception 1995, 24S:38.
46. 46. Polat U, Sagi D, Norcia AM: Abnormal spatial interactions in amblyopia. Vision Res 1997, 37:737-744.
47. 47. Kovacs I, Polat U, Norcia AM: Breakdown of binding mechanisms in amblyopia. Invest Ophthalmol Vis Sci 1996, 37S:670.
48. 48. Hess RF, McIlhagga W, Field DJ: Contour integration in strabismic amblyopia: the sufficiency of an explanation based on positional uncertainty. Vision Res 1997, 37:3145-3161. This paper extends the study of the basic spatial deficits in amblyopia to the level of perceptual integration. The authors asked strabismic amblyopes to locate a coherent contour amid noise composed of elements of the same form as the contour elements. They found that the observers were impaired with their amblyopic eye over a wide range of element orientations and contrasts. However, in many cases, the performance of the amblyopic eye could be mimicked by adding positional jitter to the elements of the contour for the fellow eye. This supports the idea that positional uncertainty is elevated in strabismic amblyopes and highlights the associated perceptual deficits.
49. 49. Field DJ, Hayes A, Hess RF: Contour integration by the human visual system: evidence for a local 'association field'. Vision Res 1993, 33:173-193.
50. 50. Hess RF, Demanins R: Contour integration in anisometropic amblyopia. Vision Res 1998, 38:889-894. This study is similar in design to Hess et al. [48•]. The purpose was to test the idea that positional uncertainty is elevated in anisometropic as well as strabismic amblyopes. The authors found that anisometropic amblyopic eyes performed similarly to fellow eyes as long as the stimuli were equated in terms of visibility. This is a particularly interesting result because it suggests that anisometropic amblyopes do not have perceptual level organizational deficits.
51. 51. Levi DM, Sharma V: Integration of local orientation in strabismic amblyopia. Vision Res 1998, 38:775-781.
52. 52. Roelfsema PR: Solutions for the binding problem. Z Naturforsch 1998, 53:691-715. This is an interesting discussion of the 'binding problem' in visual perception. Although it is not a primary research paper, it discusses the rationale behind the attempt to link neuronal synchrony to perceptual organization functionally. Only a piece of the discussion is directly related to amblyopia, but that section puts the data on strabismus and amblyopia in perspective relative to the larger problem of feature binding.
53. 53. McKee SP, Schor CM, Steinman SB, Wilson N, Koch GG, Davis SM, Hsu-Winges C, Day SH, Chan CL, Movshon JA et al.: The classification of amblyopia on the basis of visual and oculomotor performance. Trans Am Ophthalmol Soc 1992, 90:123.
54. 54. Imamura K, Richter H, Fischer H, Lennerstrand G, Franzen O, Rydberg A, Andersson J, Schneider H, Onoe H, Watanabe Y, Langstrom B: Reduced activity in the extrastriate visual cortex of individuals with strabismic amblyopia. Neurosci Lett 1997, 225:173-176.