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Visual resolution limits in human albinism
0042-6989/91 $3.00 + 0.00 Copyright 0 1991 Pergamon Press plc
Vision Res. Vol. 31. No. 718, pp. 14454447, 1991 Printed in Great Britain. AI1 rights reserved
RESEARCH NOTE
VISUAL RESOLUTION
LIMITS IN HUMAN
RICHARD V. ABAJJI U.M.I.S.T.,
ALBINISM
and EVE PASCAL
Department of Optometry and Vision Sciences, P.O. Box 88, Manchester M60 IQD, U.K. (Received 15 August 1990; in revised form 14 November 1990)
Abstract-The effects of the involuntary ocular oscillations on visual resolution was examined in 22 albinos and 11 idiopaths with congenital nystagmus. The idiopaths showed a linear relationship between the proportion of the slow phase spent at low velocities (Q 10 deg/sec) and the log of the minimum angle of resolution; such that long dwell times were compatible with good resolution. For the albinos there appeared to be a critical duration of low retinal slip velocities above which there was no improvement in acuity. This supports the contention that factors other than the congenital nystagmus limit visual resolution in the albino. Albinism
Minimum angle of resolution
Foveal hypoplasia
INTRODUCTION
Albinism represents a heterogeneous group of inherited disorders of pigmentation and is characterized by a cluster of ocular features including congenital nystagmus, fovea1 hypoplasia, photophobia, ametropia and strabismus. In the albino population visual acuity ranges between 3/60 and about 6/12 (Taylor, 1978; Siegel, 1979; Van Dorp, 1985; Abadi, Pascal, Whittle & Worfolk, 1989). The presence of nystagmus and the lack of a normally differentiated fovea are thought to be primarily responsible for this reduction in spatial resolution (Dickinson & Abadi, 1985; Wilson, Mets, Nagy & Kressel, 1988a). The effect of congenital nystagmus on visual performance is dictated by the retinal slip velocities that comprise each slow phase and, in particular, the duration of the period in which the retinal velocity is reasonably slow (Dell’Osso, 1973; Abadi & Sandikcioglu, 1974; Dell’Osso & Daroff, 1975). As part of a recent study Abadi and Worfolk (1989) demonstrated that, for a group of subjects with idiopathic nystagmus, there was a significant correlation between the log of the minimum angle of resolution (logMAR) and the percentage of time spent at or below lOdeg/sec. The aim of this study was to investigate this relationship in a group of albinos, so that the independent effects of involuntary ocular
Nystagmus
oscillations and fovea1 hypoplasia resolution limits could be assessed.
on visual
METHODS
The horizontal eye movements of 22 albinos and 11 idiopaths with congenital nystagmus were recorded with an i.r. limbal reflection technique, whilst they fixated a circular stationary target (0.2 deg) in primary gaze. The albino group comprised 10 tyrosinase-negative oculocutaneous albinos, 7 tyrosinase-positive oculocutaneous albinos, 3 x-linked ocular albinos and 2 autosomal-recessive ocular albinos. Eye position data were stored on a frequency-modulated tape recorder and then digitized to 8 bit accuracy at 500 Hz with a BBC master computer. For each subject a representative 10 set of data was selected for slow phase analysis. The exceptions to this were those with periodic alternating nystagmus (10 albinos and 2 idiopaths), for whom 10 set of both right-beating and left-beating nystagmus were analyzed before the results were combined. Slow phases were sampled at 250 Hz and then digitally filtered with a non-recursive quadratic filter (- 3 dB at 23 Hz), as described by Abadi and Worfolk (1989). In order to avoid the inclusion of any fast phases in this analysis all fast phase data, from 8 msec before until 8 msec after the point at which the saccadic velocity
1445
Research Note
1446
reached 40 deg/sec, were eliminated. Velocities, derived from a two point central difference algorithm, were then sampled at 12.5 msec intervals along the slowphase. Binocular visual acuity was measured with a high contrast (90%) Bailey-Lovie chart located in the primary position. RESULTS AND DISCUSSION
Visual resolution in our group of 22 albinos ranged from 0.92 to 0.52 logMAR (Snellen equivalents 6/48 to 6/19-l), which is in accord with the resolution limits measured in other studies. Generally the tyrosinase-negative oculocutaneous albinos had lower acuities than either the tyrosinase-positive or ocular albinos. This inverse relationship, between the degree of fundus hypopigmentation and the level of acuity, has been documented in the past (Witkop, 1979; O’Donnell & Green, 1981; Kinnear, Jay & Witkop, 1985; Van Dorp, 1985; Abadi & Pascal, 1989). Amongst our subjects with congenital idiopathic nystagmus, acuity varied from 0.66 to 0 logMAR (Snellen values of 6/30+2 to 6/6). All of the subjects exhibited an involuntary nystagmus that was conjugate and in the horizontal plane. In Fig. 1 the relationship between logMAR visual acuity and the percentage of time that slow phase velocity was less than or equal to 10 deg/sec is shown for both the albinos (open symbols) and the idiopaths (solid symbols). From this graph it can be seen that, for the
Fig. I. The relationship between the log of the minimum angle of resolution (logMAR) and the percentage of time that nystagmus slow phase velocity was less than or equal to 10 deg/sec. Open symbols (0) represent the data from 22 albino subjects, with a best tit exponential curve. Solid symbols (a) represent data from 11subjects with idiopathic congenital nystagmus. The straight line shows the least squares best fit to these data points (r = -0.76, P c: 0.01).
idiopaths, the level of acuity improved as the proportion of time spent at low velocities (the “dwell time”) increased. The correlation between these two parameters was found to be statistically significant (r = -0.76: P < 0.01). Albino visual acuity (which tended to be lower than that of the idiopaths) was also related to the percentage of time spent at velocities of 10 deg/sec or less, however this relationship was not linear. Instead, acuity improved as the proportion of dwell time increased only up to a resolution limit of about 0.52. Any further increase in the duration of low retinal slip velocities did not result in better visual acuity. Thus, as previously suggested, visual resolution in albinism appears to be limited by factors other than the ongoing congenital nystagmus (Collewijn, Apkarian & Spekreijse, 1985; Dickinson & Abadi, 1985; Wilson et al., 1988a). Evidence of the absence of normal fovea1 differentiation in albinism was first provided by Nettleship (1906) and Usher (1920). Since then histological studies have reported that the ganglion cell layer appears to be continuous throughout the retina and a rod-free area is not identifiable in the albino fundus (Naumann, 1976; O’Donnell, Lerche & Schroeder, Hambrick, Green, Iliff & Stone, 1976; Fulton, Albert & Craft, 1978). Fovea1 hypoplasia has also been documented in an albino green monkey (Guillery, Hickey, Kaas, Felleman, Debruyn & Sparks, 1984). Recent psychophysical evaluation of albino spatiotemporal visual performance has indicated that peripheral vision is essentially normal, whilst central vision seems to be limited by the lower receptor density and (to a lesser extent) the reduced central cone outer-segment length (Wilson et al., 1988a, b; Yo, Wilson, Mets & Ritacco, 1989). These results, combined with a favourable comparison between the adult albino visual system and that of a normal IO-month old infant, led Wilson and his colleagues to postulate that the deficiencies of albino spatial vision could be due to arrested central retinal development. Visual resolution in albinos appears to be limited primarily by fovea1 hypoplasia, however other ocular factors may also play a role in the reduction of visual acuity. In particular the presence of congenital nystagmus and ametropia from early infancy may be responsible for some degree of deprivational amblyopia (Abadi & King-Smith, 1979; Abadi & Dickinson, 1986). Additionally the adoption of different and variable foveation strategies
Research Note
(Abadi et al., 1989) may influence visual performance in albinism. Acknowledgements-We would like to thank Neil Charman and Ralph Worfolk for their helpful comments.
REFERENCES Abadi, R. V. & Dickinson, C. M. (1986). Waveform characteristics in congenital nystagmus. Documenta Ophfhalmolo&a 64, 153-167. Abadi, R. V. & King-Sag, P. E. (1979). Congenital nys~~us modifies orientational detection. Firion Research, 19, 1409-1411. Abadi, R. V. & Pascal, E. (1989). The recognition and management of albinism. Ophthalmic and PhysioIogical Optics, 9, 3-15. Abadi, R. V. BE Sandikcioglu, M. (1974). Electro-oculographic response in a case of bilateral idiopathic nystagmus. British Journal of Physiological Optics, 29, 73-85. Abadi, R. V. & Worfolk, R. (1989). Retinal slip velocities in congenital nystagmus. Vision Research, 29, 195-205. Abadi, R. V., Pascal, E., Whittle, J. t Worfolk, R. (1989). Retinal fixation behaviour in human albinos. Optometry and Yision Science, 66, 276-280. Collewijn, H., Apkarian, P. & Spekreijse, H. (1985). The oculomotor behaviour of human albinos. Brain, 108, l-28. Dell’Osso, L. F. (1973) Fixation characteristics in hereditary congenital nystagmus. American Journal of Optometry and Archives of the American Academy of Opfometry, SO, U-90. Dell’Osso, L. F. & Daroff, R. B. (1975). Congenital nystagmus waveforms and foveation strategy. Documenta Oph thalmoiogica, 39, 155-l 82. Dickinson, C. M. & Abadi, R. V. (1985). The influence of nystagmoid oscillation on contrast sensitivity in normal observers. Vision Research, 2% 1089-f 096. Fulton, A. B., Albert, D. M. Br Craft, J. L. (1978). Human albinism: light and electron microscopy study. Archives of Ophthaimo~ogy, %, 305-310. Guillery, R. W., Hickey, T. L., Kaas J. H., Felleman, D. J., Debruyn, E. J. & Sparks, D. L. (1984). Abnormal central
1447
visual pathways in the brain of an albino green monkey. Journal of Comparative Neurotogy~ 226, 165-183. Kinnear, P. E., Jay, 8. & Witkop, C. J. (1985). Albinism. Survey of Ophthalmology, 30, 75-101. Naumann, G. 0. II., Lerche, W. SLSchroeder, W. (1976). Foveola-Aplaaie bei Tyrosinase positivem oculocutanen Albinismus. Albrechf Von Graefes Arch Khnical und Experimentale Ophthalmoiogie, 200, 39-50. Nettleship, E. (1906). Notes on some varieties of albinism. Transactions of the Ophfhalmological Society of the U.K., 26, 244-250. O’Donnell, F. E. & Green, W. R. (1981). The eye in albinism. In Duane, T. D. (Ed.), Chnica~ophtha~o~o8y (Vol. 4, Chap. 38, pp. l-23). New York: Harper & Row. G’Donnell, F. E., Hambrick, G. W., Green, W. R., Biff, W. J. & Stone, J. L. (1976). X-linked ocular albinism: An oculocutaneous macromelanosomal disorder. Archives of Ophthalmology, 94, 1883-1892. Siegel, I. M. (1979). Ophthalmological findings in tyrosinase positive oculocutaneous albinism. Perspectives in Oph thalmology, 3, 11-23. Taylor, W. 0. G. (1978)‘Visual disabilities of oculocutaneous albinism and their alleviation. Transactions of the Ophthalmological Society of the U.K. 98, 423-445. Usher, C. H. (1920), Histological examination of an adult human albino’s eyeball with a note on mesoblastic pigmentation in foetal eyes. Bio~tr~a, 13, 45-56. Van Dorp, D. B. (1985). Shades of grey in human albinism. Amersfoort. The Netherlands: Holland Ophthalmic Publishing Centre. Wilson, H. R., Mets, M. B., Nagy, S. E. & Kressel, A. B. (1988a) Albino spatial vision as an instance of arrested visual development. Vision Research, 28, 979-990. Wilson, H. R., Mets, M. B., Nagy, S. E. & Ferrera, V. P. (1988b) Spatial frequency and orientation tuning of spatial visual mechanisms in human albinos. Vision Research, 28, 991-999. Witkop, C. J. (1979). Depigmenfations of the general and oral tissues and their genetic foundations. Alabama Journal of Medical Science, Id, 331-343. Yo, C., Wilson, H. R., Mets, M. B. & Ritacco, D. G. (1989). Human albinos can discriminate spatial frequency and phase as accurately as normal subjects. Vision Research, 29, 1561-1574.
Vision Res. Vol. 31. No. 718, pp. 14454447, 1991 Printed in Great Britain. AI1 rights reserved
RESEARCH NOTE
VISUAL RESOLUTION
LIMITS IN HUMAN
RICHARD V. ABAJJI U.M.I.S.T.,
ALBINISM
and EVE PASCAL
Department of Optometry and Vision Sciences, P.O. Box 88, Manchester M60 IQD, U.K. (Received 15 August 1990; in revised form 14 November 1990)
Abstract-The effects of the involuntary ocular oscillations on visual resolution was examined in 22 albinos and 11 idiopaths with congenital nystagmus. The idiopaths showed a linear relationship between the proportion of the slow phase spent at low velocities (Q 10 deg/sec) and the log of the minimum angle of resolution; such that long dwell times were compatible with good resolution. For the albinos there appeared to be a critical duration of low retinal slip velocities above which there was no improvement in acuity. This supports the contention that factors other than the congenital nystagmus limit visual resolution in the albino. Albinism
Minimum angle of resolution
Foveal hypoplasia
INTRODUCTION
Albinism represents a heterogeneous group of inherited disorders of pigmentation and is characterized by a cluster of ocular features including congenital nystagmus, fovea1 hypoplasia, photophobia, ametropia and strabismus. In the albino population visual acuity ranges between 3/60 and about 6/12 (Taylor, 1978; Siegel, 1979; Van Dorp, 1985; Abadi, Pascal, Whittle & Worfolk, 1989). The presence of nystagmus and the lack of a normally differentiated fovea are thought to be primarily responsible for this reduction in spatial resolution (Dickinson & Abadi, 1985; Wilson, Mets, Nagy & Kressel, 1988a). The effect of congenital nystagmus on visual performance is dictated by the retinal slip velocities that comprise each slow phase and, in particular, the duration of the period in which the retinal velocity is reasonably slow (Dell’Osso, 1973; Abadi & Sandikcioglu, 1974; Dell’Osso & Daroff, 1975). As part of a recent study Abadi and Worfolk (1989) demonstrated that, for a group of subjects with idiopathic nystagmus, there was a significant correlation between the log of the minimum angle of resolution (logMAR) and the percentage of time spent at or below lOdeg/sec. The aim of this study was to investigate this relationship in a group of albinos, so that the independent effects of involuntary ocular
Nystagmus
oscillations and fovea1 hypoplasia resolution limits could be assessed.
on visual
METHODS
The horizontal eye movements of 22 albinos and 11 idiopaths with congenital nystagmus were recorded with an i.r. limbal reflection technique, whilst they fixated a circular stationary target (0.2 deg) in primary gaze. The albino group comprised 10 tyrosinase-negative oculocutaneous albinos, 7 tyrosinase-positive oculocutaneous albinos, 3 x-linked ocular albinos and 2 autosomal-recessive ocular albinos. Eye position data were stored on a frequency-modulated tape recorder and then digitized to 8 bit accuracy at 500 Hz with a BBC master computer. For each subject a representative 10 set of data was selected for slow phase analysis. The exceptions to this were those with periodic alternating nystagmus (10 albinos and 2 idiopaths), for whom 10 set of both right-beating and left-beating nystagmus were analyzed before the results were combined. Slow phases were sampled at 250 Hz and then digitally filtered with a non-recursive quadratic filter (- 3 dB at 23 Hz), as described by Abadi and Worfolk (1989). In order to avoid the inclusion of any fast phases in this analysis all fast phase data, from 8 msec before until 8 msec after the point at which the saccadic velocity
1445
Research Note
1446
reached 40 deg/sec, were eliminated. Velocities, derived from a two point central difference algorithm, were then sampled at 12.5 msec intervals along the slowphase. Binocular visual acuity was measured with a high contrast (90%) Bailey-Lovie chart located in the primary position. RESULTS AND DISCUSSION
Visual resolution in our group of 22 albinos ranged from 0.92 to 0.52 logMAR (Snellen equivalents 6/48 to 6/19-l), which is in accord with the resolution limits measured in other studies. Generally the tyrosinase-negative oculocutaneous albinos had lower acuities than either the tyrosinase-positive or ocular albinos. This inverse relationship, between the degree of fundus hypopigmentation and the level of acuity, has been documented in the past (Witkop, 1979; O’Donnell & Green, 1981; Kinnear, Jay & Witkop, 1985; Van Dorp, 1985; Abadi & Pascal, 1989). Amongst our subjects with congenital idiopathic nystagmus, acuity varied from 0.66 to 0 logMAR (Snellen values of 6/30+2 to 6/6). All of the subjects exhibited an involuntary nystagmus that was conjugate and in the horizontal plane. In Fig. 1 the relationship between logMAR visual acuity and the percentage of time that slow phase velocity was less than or equal to 10 deg/sec is shown for both the albinos (open symbols) and the idiopaths (solid symbols). From this graph it can be seen that, for the
Fig. I. The relationship between the log of the minimum angle of resolution (logMAR) and the percentage of time that nystagmus slow phase velocity was less than or equal to 10 deg/sec. Open symbols (0) represent the data from 22 albino subjects, with a best tit exponential curve. Solid symbols (a) represent data from 11subjects with idiopathic congenital nystagmus. The straight line shows the least squares best fit to these data points (r = -0.76, P c: 0.01).
idiopaths, the level of acuity improved as the proportion of time spent at low velocities (the “dwell time”) increased. The correlation between these two parameters was found to be statistically significant (r = -0.76: P < 0.01). Albino visual acuity (which tended to be lower than that of the idiopaths) was also related to the percentage of time spent at velocities of 10 deg/sec or less, however this relationship was not linear. Instead, acuity improved as the proportion of dwell time increased only up to a resolution limit of about 0.52. Any further increase in the duration of low retinal slip velocities did not result in better visual acuity. Thus, as previously suggested, visual resolution in albinism appears to be limited by factors other than the ongoing congenital nystagmus (Collewijn, Apkarian & Spekreijse, 1985; Dickinson & Abadi, 1985; Wilson et al., 1988a). Evidence of the absence of normal fovea1 differentiation in albinism was first provided by Nettleship (1906) and Usher (1920). Since then histological studies have reported that the ganglion cell layer appears to be continuous throughout the retina and a rod-free area is not identifiable in the albino fundus (Naumann, 1976; O’Donnell, Lerche & Schroeder, Hambrick, Green, Iliff & Stone, 1976; Fulton, Albert & Craft, 1978). Fovea1 hypoplasia has also been documented in an albino green monkey (Guillery, Hickey, Kaas, Felleman, Debruyn & Sparks, 1984). Recent psychophysical evaluation of albino spatiotemporal visual performance has indicated that peripheral vision is essentially normal, whilst central vision seems to be limited by the lower receptor density and (to a lesser extent) the reduced central cone outer-segment length (Wilson et al., 1988a, b; Yo, Wilson, Mets & Ritacco, 1989). These results, combined with a favourable comparison between the adult albino visual system and that of a normal IO-month old infant, led Wilson and his colleagues to postulate that the deficiencies of albino spatial vision could be due to arrested central retinal development. Visual resolution in albinos appears to be limited primarily by fovea1 hypoplasia, however other ocular factors may also play a role in the reduction of visual acuity. In particular the presence of congenital nystagmus and ametropia from early infancy may be responsible for some degree of deprivational amblyopia (Abadi & King-Smith, 1979; Abadi & Dickinson, 1986). Additionally the adoption of different and variable foveation strategies
Research Note
(Abadi et al., 1989) may influence visual performance in albinism. Acknowledgements-We would like to thank Neil Charman and Ralph Worfolk for their helpful comments.
REFERENCES Abadi, R. V. & Dickinson, C. M. (1986). Waveform characteristics in congenital nystagmus. Documenta Ophfhalmolo&a 64, 153-167. Abadi, R. V. & King-Sag, P. E. (1979). Congenital nys~~us modifies orientational detection. Firion Research, 19, 1409-1411. Abadi, R. V. & Pascal, E. (1989). The recognition and management of albinism. Ophthalmic and PhysioIogical Optics, 9, 3-15. Abadi, R. V. BE Sandikcioglu, M. (1974). Electro-oculographic response in a case of bilateral idiopathic nystagmus. British Journal of Physiological Optics, 29, 73-85. Abadi, R. V. & Worfolk, R. (1989). Retinal slip velocities in congenital nystagmus. Vision Research, 29, 195-205. Abadi, R. V., Pascal, E., Whittle, J. t Worfolk, R. (1989). Retinal fixation behaviour in human albinos. Optometry and Yision Science, 66, 276-280. Collewijn, H., Apkarian, P. & Spekreijse, H. (1985). The oculomotor behaviour of human albinos. Brain, 108, l-28. Dell’Osso, L. F. (1973) Fixation characteristics in hereditary congenital nystagmus. American Journal of Optometry and Archives of the American Academy of Opfometry, SO, U-90. Dell’Osso, L. F. & Daroff, R. B. (1975). Congenital nystagmus waveforms and foveation strategy. Documenta Oph thalmoiogica, 39, 155-l 82. Dickinson, C. M. & Abadi, R. V. (1985). The influence of nystagmoid oscillation on contrast sensitivity in normal observers. Vision Research, 2% 1089-f 096. Fulton, A. B., Albert, D. M. Br Craft, J. L. (1978). Human albinism: light and electron microscopy study. Archives of Ophthaimo~ogy, %, 305-310. Guillery, R. W., Hickey, T. L., Kaas J. H., Felleman, D. J., Debruyn, E. J. & Sparks, D. L. (1984). Abnormal central
1447
visual pathways in the brain of an albino green monkey. Journal of Comparative Neurotogy~ 226, 165-183. Kinnear, P. E., Jay, 8. & Witkop, C. J. (1985). Albinism. Survey of Ophthalmology, 30, 75-101. Naumann, G. 0. II., Lerche, W. SLSchroeder, W. (1976). Foveola-Aplaaie bei Tyrosinase positivem oculocutanen Albinismus. Albrechf Von Graefes Arch Khnical und Experimentale Ophthalmoiogie, 200, 39-50. Nettleship, E. (1906). Notes on some varieties of albinism. Transactions of the Ophfhalmological Society of the U.K., 26, 244-250. O’Donnell, F. E. & Green, W. R. (1981). The eye in albinism. In Duane, T. D. (Ed.), Chnica~ophtha~o~o8y (Vol. 4, Chap. 38, pp. l-23). New York: Harper & Row. G’Donnell, F. E., Hambrick, G. W., Green, W. R., Biff, W. J. & Stone, J. L. (1976). X-linked ocular albinism: An oculocutaneous macromelanosomal disorder. Archives of Ophthalmology, 94, 1883-1892. Siegel, I. M. (1979). Ophthalmological findings in tyrosinase positive oculocutaneous albinism. Perspectives in Oph thalmology, 3, 11-23. Taylor, W. 0. G. (1978)‘Visual disabilities of oculocutaneous albinism and their alleviation. Transactions of the Ophthalmological Society of the U.K. 98, 423-445. Usher, C. H. (1920), Histological examination of an adult human albino’s eyeball with a note on mesoblastic pigmentation in foetal eyes. Bio~tr~a, 13, 45-56. Van Dorp, D. B. (1985). Shades of grey in human albinism. Amersfoort. The Netherlands: Holland Ophthalmic Publishing Centre. Wilson, H. R., Mets, M. B., Nagy, S. E. & Kressel, A. B. (1988a) Albino spatial vision as an instance of arrested visual development. Vision Research, 28, 979-990. Wilson, H. R., Mets, M. B., Nagy, S. E. & Ferrera, V. P. (1988b) Spatial frequency and orientation tuning of spatial visual mechanisms in human albinos. Vision Research, 28, 991-999. Witkop, C. J. (1979). Depigmenfations of the general and oral tissues and their genetic foundations. Alabama Journal of Medical Science, Id, 331-343. Yo, C., Wilson, H. R., Mets, M. B. & Ritacco, D. G. (1989). Human albinos can discriminate spatial frequency and phase as accurately as normal subjects. Vision Research, 29, 1561-1574.