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Local Adaptation in Functional Amblyopia
LOCAL A D A P T A T I O N I N F U N C T I O N A L AMBLYOPIA T E D LAWV ULL, M . D .
Louisville, Kentucky
Also implicit in the application of the con cept of local adaptation to functional am blyopia are two other ideas. One is that if local adaptation were the only cause of this amblyopia, then the visual acuity of am blyopic and of normal eyes should be equal at extremely short target exposure times. The other is that if local adaptation is in volved in functional amblyopia, then this phenomenon should be measurably different in amblyopic eyes, compared with normal eyes. This report describes three experiments. A loose correlation between eye move ments, dark-adaptation, and visual acuity has The first deals with the fixation patterns of been shown to exist in functional amblyopia. amblyopic and of normal eyes and correlates It has been noted that fixation patterns in subjective phenomena with these patterns; the amblyope are poorest at high levels of il the second deals with a comparison of visual lumination, whereas there is little difference acuities between amblyopic and normal eyes, between the fixation patterns at medium- using short target exposure times; and the light levels and those of the dark-adapted third deals with comparison of local adapta state.4 It has been noted further that in the tion between amblyopic and normal eyes de amblyopic eye, vision is better at medium- termined psychophysically. light levels than at higher levels, while in the dark-adapted state the amblyopic eye has vi EXPERIMENT 1. FIXATION PATTERNS AND sion as good as that of the normal eye in the SUBJECTIVE PHENOMENA same state.8
Patients with strabismic functional am blyopia often describe unusual visual phe nomena while their visual acuity is being tested. For instance, they may comment, "It seems clear when I first look at it, but it fades out before I can read it." Or, "I rec ognize several letters in the line, but I can't say where they fall in the line." Or, "I see two letters on top of each other." Or, "I can read the first letter in the line, but not the ones in between." Pugh 1 3 has described most of these phenomena comprehensively.
There is reason to suspect that a sort of "local adaptation" may play a role in stra bismic amblyopia, and further, that eye move ments may produce temporary, fleeting im provements in this amblyopic vision. Local adaptation is defined as the adaptation of just one area of the visual field to a steady stimulus, so that awareness of that stimulus decreases or stops. Implicit in this is the cor ollary that when a stimulus is moving, awareness of it will not cease. From the ERG Laboratory of the Department of Ophthalmology and the Neurosensory Center (Pub lication No. 130) of the College of Medicine of the University of Iowa. The work of the ERG Labora tory is supported by Grant B-349; and the Neuro sensory Center, by Program Project Grant B-3354 of the National Institute of Neurologic Diseases and Blindness, National Institutes of Health, Bethesda, Maryland.
MATERIAL AND METHOD
The apparatus consisted of an infrared indirect ophthalmoscope with a marker at the level of the fundus image with which to compare fundus movement, and a glass re flecting plate between the objective lens of the ophthalmoscope and the patient's eye (fig. 1). Reflected in this plate from 20 feet was a standard clinic visual acuity chart, il luminated by a light. The intensity of the light could be varied. This allowed the subject to observe the visual acuity chart monocularly while the examiner studied any changes in direction of that eye through the reflecting plate which was transparent to infrared rays. Thus, the experimenter was able to correlate the eye movements with his acuity reports. Movements of three minutes of arc were easily seen when the marker was placed over
904
AMERICAN JOURNAL OF OPHTHALMOLOGY
JUNE, 1968
Fig. 1 (Lawwill). The infrared indirect ophthalmoscope. On the left supporting bar is the infrared image converter tube and its telescope. In the center above is the light source and infrared filter. On the right sup porting bar is the sighting target for the examiner. At the end of the right bar is the objective lens of the indirect ophthalmoscope and the rec tangular glass plate in which the subject observed the reflected acuity chart. The subject's chin rest is at the right.
the image of a vessel. Calibration consisted of comparing the distance change between the marker and the vessel with a fixation change on the chart equivalent to 20 or 30 minutes. RESULTS
In eight patients, fixation patterns of the amblyopic eyes were obviously quite differ ent from those of the normal fellow eyes. Whereas the normal eye was able to hold fix ation on the target for most of the assigned time, with occasional "drifts" from the tar get of from 6 to 20 minutes of arc, the am blyopic eye showed a much different pattern. The initial fixation was maintained for a brief period, and then the eye would drift off horizontally, sometimes as much as two de grees of arc, then return to the target. Sub sequent duration of fixation was progres sively shorter, with drifts more frequent. Eyes with the most profound amblyopia showed the shortest periods of fixation and the greatest arcs of drift. After a rest of several seconds the whole cycle would repeat itself. There was a correlation between the pa
tient's reporting a fading image and the drifting observed through the ophthalmo scope. The fading was described as the drift ing motion started. The image was described as reappearing at the terminus of the drift. When restitution to the initial fixation point occurred, the patients stated that at that point they were aware that an involuntary eye movement had occurred. DISCUSSION
If the objective and subjective phenomena are related, there are three possible assump tions: either the fading phenomenon results from the drifting of the eye, or the eye drifts because the image has faded, or both are dependent upon a third variable. Since optically stabilized images fade quite rapidly when drift is compensated, it seems unlikely that drift initiates the fade. When images are optically stabilized the pattern of drifts is changed, implying that if both are depen dent upon a third variable, this third variable is affected by image-fading. It may be that the poor fixation pattern of amblyopic eyes is partially due to the fact that their local ad aptation is more rapid than normal.
VOL. 65, NO. 6
FUNCTIONAL AMBLYOPIA
EXPERIMENT 2. VISUAL ACUITY AT SHORT EXPOSURE TIMES MATERIAL AND METHOD
A double tachistoscope, consisting of two projectors mounted on the sanie base and fo cused at the same area of a common screen, was synchronized so that when the shutter on either projector was open the shutter on the other was closed. The test projector was adjusted for exposure times of variable length between 10 and 1,000 milliseconds. The other projector kept the screen illumi nated at a constant and equal level between test exposures. Test exposures were made at progressively increasing exposure times, and the target size increased until identification was made by the subject. The target was a letter E in varying orientations, and identifi cation consisted of correctly naming the ori entation. Using this method, acuities were measured monocularly at exposure times of 10, 20, 40, 100, 200, 500 and 1,000 millise conds in both normal and amblyopic eyes, with the other eye covered. RESULTS
The data are inconclusive at these expo sure times. There is an apparent equal dimi nution of acuity in both the amblyopic and normal eyes as exposure times become shorter. DISCUSSION
If local adaptation accounts in part for the decrease in visual acuity in amblyopia, the difference in acuity between the normal and amblyopic eye should be less at shorter exposure times. If fading explains the greater crowding phenomenon in amblyopia, linear and single letter acuity should be simi lar at shorter exposure times. At exposure times used, this could not be substantiated. Equipment limitations precluded shorter ex posures. EXPERIMENT 3. LOCAL ADAPTATION MATERIAL AND METHOD
Instead of an optically stabilized retinal image, the technique used in this experiment
90S
involved constant voluntary fixation of a specified target. A slide was devised for a major amblyoscope consisting of an opaque field with two holes. When viewed in the amblyoscope, the holes were 1.7 degrees in diameter and separated along the same hori zontal line by 5.7 degrees of arc. One hole was covered by a red filter, while the other was left clear. The luminance through the red hole was 31 footlamberts, while that of the clear was 470 footlamberts. The slide was placed in the amblyoscope so that as each eye was tested the red hole was seen temporal to the clear. The directions to the subjects were the following: 1. Stare at the clear circle until the red circle disappears, and indicate by tapping the finger when this occurs. 2. Stare at the red circle until the clear circle disappears, and indicate by tapping the finger when this occurs. 3. Stare at the red circle until the red cir cle itself disappears, and indicate by tapping the finger when this occurs. RESULTS
A comparison between the results in nor mal and in amblyopic eyes is presented nu merically in Table 1. An interesting observa tion by subjects in the course of this experi ment was that in the performance of the sec ond assigned task, the red fixation circle sometimes disappeared before the clear circle did. This occurred in amblyopic eyes only. DISCUSSION
The results indicate that when measured in this manner, local adaptation is signifi cantly accelerated in some amblyopic eyes, as compared with the normal fellow eyes. This is true not only in the region of fixation, bul as far as 5.7 degrees away from it horizon tally in either direction. In some cases (Sub jects 5 and 6) this difference was less marked, and it is of interest that both oi these subjects were undergoing good-eyeocclusion therapy at the time of these ex periments, indicating that the acceleration oi local adaptation which has been ascribed tc
906
AMERICAN JOURNAL OF OPHTHALMOLOGY
JUNE, 1968
TABLE 1 DISAPPEARANCE TIME IN SECONDS FOR STEADILY FIXATED TARGETS IN NORMAL AND AMBLYOPIC EYES OF SEVEN PATIENTS*
Normal 1. 2. 3. 4. 5. 6. 7.
6/6 6/9 6/6 6/6 6/6 6/6 6/6
B
A
Visual Acuity
C
Amblyopic
Normal
Amblyopic
Normal
Amblyopic
Normal
Amblyopic
5/60 6/60 6/30 6/60 6/21 6/21 6/6f
20 20 9 17 16 9 28f
25 Central first 7 7 12 8 24t
29 37 38 >45 11 9 40 f
12 Central first 7 16 18 7 35 f
>55 >55 >45 55 40 11 >55f
17 11 9 35 33 11 >55f
* Targets were 1.7° in diameter and 5.7° apart. The red target was always temporal to the white and of lower intensity. In Column A are times in seconds for disappearance of red target when fixing on the white one. In Column B are times in seconds for disappearance of the white target while fixating the red one. In Column C are times m seconds for disappearance of the red target while fixing on it. t Normal patient.
functional amblyopia is, to at least some ex tent, reversible, or can be accentuated in the normal eye by occlusion. CONCLUSIONS
The experiments described here indicate that there is an accelerated local adaptation in the central and paracentral regions of the visual field of amblyopic eyes. Further, this local adaptation is related to the differences noted subjectively between amblyopic and normal eyes in the vision-testing situation. However, these experiments also indicate that this accelerated local adaptation is not solely responsible for the poor vision which can be measured in these eyes. In fact, to a limited degree the results of one of these ex periments indicate that the local adaptation may be completely unrelated to the poor vi sion. There is the possibility that adaptation in the amblyopic eye is potentiated by the al most constant state of supression in that eye, thus adding another facet to local adaptation. SUMMARY
Three experiments dealing with compari sons between amblyopic and normal eyes are described. The first demonstrated that the fixation pattern of amblyopic eyes differs from that of normal eyes. The timing of the different subjective phenomena noted in these eyes can be correlated with the timing of fix
ation events. In the second experiment it was not possible to demonstrate that as ex posure time of acuity targets is reduced when comparing amblyopic with normal eyes, the respective visual acuities of the two eyes tend to become similar. In the third experi ment it was demonstrated that local adapta tion proceeds faster in the central and para central region of the amblyopic eye than in the normal fellow eye. Department of Ophthalmology University of Louisville School of Medicine 323 Chestnut Street (20402) ACKNOWLEDGMENTS
I should like to thank Dr. Hermann Burian for the opportunity of working in his laboratory, and LTC Budd Appleton for his review of the paper. REFERENCES
1. Pugh, M.: Brightness perception and binocular adaptation. Brit. J. Ophth. 35:134, 1951. 2. Pugh, M.: Foveal vision in amblyopia. Brit. J. Ophth. 38:321, 1954. 3. Pugh, M.: Visual distortion in amblyopia. Brit. J. Ophth. 42 :449, 1958. 4. Lawwill, T.: The fixation pattern of the light-adapted and dark-adapted amblyopic eye. Am. J. Ophth. 61:1416, 1966. 5. Lawwill, T. and Burian, H. M.: Luminance, contrast function and visual acuity in functional amblyopia. Am. J. Ophth. 62:511, 1966. 6. Stuart, J. A. and Burian, H. M.: A study of separation difficulty: Its relationship to visual acuity in normal and amblyopic eyes. Am. J. Ophth. 53:471, 1962.
Louisville, Kentucky
Also implicit in the application of the con cept of local adaptation to functional am blyopia are two other ideas. One is that if local adaptation were the only cause of this amblyopia, then the visual acuity of am blyopic and of normal eyes should be equal at extremely short target exposure times. The other is that if local adaptation is in volved in functional amblyopia, then this phenomenon should be measurably different in amblyopic eyes, compared with normal eyes. This report describes three experiments. A loose correlation between eye move ments, dark-adaptation, and visual acuity has The first deals with the fixation patterns of been shown to exist in functional amblyopia. amblyopic and of normal eyes and correlates It has been noted that fixation patterns in subjective phenomena with these patterns; the amblyope are poorest at high levels of il the second deals with a comparison of visual lumination, whereas there is little difference acuities between amblyopic and normal eyes, between the fixation patterns at medium- using short target exposure times; and the light levels and those of the dark-adapted third deals with comparison of local adapta state.4 It has been noted further that in the tion between amblyopic and normal eyes de amblyopic eye, vision is better at medium- termined psychophysically. light levels than at higher levels, while in the dark-adapted state the amblyopic eye has vi EXPERIMENT 1. FIXATION PATTERNS AND sion as good as that of the normal eye in the SUBJECTIVE PHENOMENA same state.8
Patients with strabismic functional am blyopia often describe unusual visual phe nomena while their visual acuity is being tested. For instance, they may comment, "It seems clear when I first look at it, but it fades out before I can read it." Or, "I rec ognize several letters in the line, but I can't say where they fall in the line." Or, "I see two letters on top of each other." Or, "I can read the first letter in the line, but not the ones in between." Pugh 1 3 has described most of these phenomena comprehensively.
There is reason to suspect that a sort of "local adaptation" may play a role in stra bismic amblyopia, and further, that eye move ments may produce temporary, fleeting im provements in this amblyopic vision. Local adaptation is defined as the adaptation of just one area of the visual field to a steady stimulus, so that awareness of that stimulus decreases or stops. Implicit in this is the cor ollary that when a stimulus is moving, awareness of it will not cease. From the ERG Laboratory of the Department of Ophthalmology and the Neurosensory Center (Pub lication No. 130) of the College of Medicine of the University of Iowa. The work of the ERG Labora tory is supported by Grant B-349; and the Neuro sensory Center, by Program Project Grant B-3354 of the National Institute of Neurologic Diseases and Blindness, National Institutes of Health, Bethesda, Maryland.
MATERIAL AND METHOD
The apparatus consisted of an infrared indirect ophthalmoscope with a marker at the level of the fundus image with which to compare fundus movement, and a glass re flecting plate between the objective lens of the ophthalmoscope and the patient's eye (fig. 1). Reflected in this plate from 20 feet was a standard clinic visual acuity chart, il luminated by a light. The intensity of the light could be varied. This allowed the subject to observe the visual acuity chart monocularly while the examiner studied any changes in direction of that eye through the reflecting plate which was transparent to infrared rays. Thus, the experimenter was able to correlate the eye movements with his acuity reports. Movements of three minutes of arc were easily seen when the marker was placed over
904
AMERICAN JOURNAL OF OPHTHALMOLOGY
JUNE, 1968
Fig. 1 (Lawwill). The infrared indirect ophthalmoscope. On the left supporting bar is the infrared image converter tube and its telescope. In the center above is the light source and infrared filter. On the right sup porting bar is the sighting target for the examiner. At the end of the right bar is the objective lens of the indirect ophthalmoscope and the rec tangular glass plate in which the subject observed the reflected acuity chart. The subject's chin rest is at the right.
the image of a vessel. Calibration consisted of comparing the distance change between the marker and the vessel with a fixation change on the chart equivalent to 20 or 30 minutes. RESULTS
In eight patients, fixation patterns of the amblyopic eyes were obviously quite differ ent from those of the normal fellow eyes. Whereas the normal eye was able to hold fix ation on the target for most of the assigned time, with occasional "drifts" from the tar get of from 6 to 20 minutes of arc, the am blyopic eye showed a much different pattern. The initial fixation was maintained for a brief period, and then the eye would drift off horizontally, sometimes as much as two de grees of arc, then return to the target. Sub sequent duration of fixation was progres sively shorter, with drifts more frequent. Eyes with the most profound amblyopia showed the shortest periods of fixation and the greatest arcs of drift. After a rest of several seconds the whole cycle would repeat itself. There was a correlation between the pa
tient's reporting a fading image and the drifting observed through the ophthalmo scope. The fading was described as the drift ing motion started. The image was described as reappearing at the terminus of the drift. When restitution to the initial fixation point occurred, the patients stated that at that point they were aware that an involuntary eye movement had occurred. DISCUSSION
If the objective and subjective phenomena are related, there are three possible assump tions: either the fading phenomenon results from the drifting of the eye, or the eye drifts because the image has faded, or both are dependent upon a third variable. Since optically stabilized images fade quite rapidly when drift is compensated, it seems unlikely that drift initiates the fade. When images are optically stabilized the pattern of drifts is changed, implying that if both are depen dent upon a third variable, this third variable is affected by image-fading. It may be that the poor fixation pattern of amblyopic eyes is partially due to the fact that their local ad aptation is more rapid than normal.
VOL. 65, NO. 6
FUNCTIONAL AMBLYOPIA
EXPERIMENT 2. VISUAL ACUITY AT SHORT EXPOSURE TIMES MATERIAL AND METHOD
A double tachistoscope, consisting of two projectors mounted on the sanie base and fo cused at the same area of a common screen, was synchronized so that when the shutter on either projector was open the shutter on the other was closed. The test projector was adjusted for exposure times of variable length between 10 and 1,000 milliseconds. The other projector kept the screen illumi nated at a constant and equal level between test exposures. Test exposures were made at progressively increasing exposure times, and the target size increased until identification was made by the subject. The target was a letter E in varying orientations, and identifi cation consisted of correctly naming the ori entation. Using this method, acuities were measured monocularly at exposure times of 10, 20, 40, 100, 200, 500 and 1,000 millise conds in both normal and amblyopic eyes, with the other eye covered. RESULTS
The data are inconclusive at these expo sure times. There is an apparent equal dimi nution of acuity in both the amblyopic and normal eyes as exposure times become shorter. DISCUSSION
If local adaptation accounts in part for the decrease in visual acuity in amblyopia, the difference in acuity between the normal and amblyopic eye should be less at shorter exposure times. If fading explains the greater crowding phenomenon in amblyopia, linear and single letter acuity should be simi lar at shorter exposure times. At exposure times used, this could not be substantiated. Equipment limitations precluded shorter ex posures. EXPERIMENT 3. LOCAL ADAPTATION MATERIAL AND METHOD
Instead of an optically stabilized retinal image, the technique used in this experiment
90S
involved constant voluntary fixation of a specified target. A slide was devised for a major amblyoscope consisting of an opaque field with two holes. When viewed in the amblyoscope, the holes were 1.7 degrees in diameter and separated along the same hori zontal line by 5.7 degrees of arc. One hole was covered by a red filter, while the other was left clear. The luminance through the red hole was 31 footlamberts, while that of the clear was 470 footlamberts. The slide was placed in the amblyoscope so that as each eye was tested the red hole was seen temporal to the clear. The directions to the subjects were the following: 1. Stare at the clear circle until the red circle disappears, and indicate by tapping the finger when this occurs. 2. Stare at the red circle until the clear circle disappears, and indicate by tapping the finger when this occurs. 3. Stare at the red circle until the red cir cle itself disappears, and indicate by tapping the finger when this occurs. RESULTS
A comparison between the results in nor mal and in amblyopic eyes is presented nu merically in Table 1. An interesting observa tion by subjects in the course of this experi ment was that in the performance of the sec ond assigned task, the red fixation circle sometimes disappeared before the clear circle did. This occurred in amblyopic eyes only. DISCUSSION
The results indicate that when measured in this manner, local adaptation is signifi cantly accelerated in some amblyopic eyes, as compared with the normal fellow eyes. This is true not only in the region of fixation, bul as far as 5.7 degrees away from it horizon tally in either direction. In some cases (Sub jects 5 and 6) this difference was less marked, and it is of interest that both oi these subjects were undergoing good-eyeocclusion therapy at the time of these ex periments, indicating that the acceleration oi local adaptation which has been ascribed tc
906
AMERICAN JOURNAL OF OPHTHALMOLOGY
JUNE, 1968
TABLE 1 DISAPPEARANCE TIME IN SECONDS FOR STEADILY FIXATED TARGETS IN NORMAL AND AMBLYOPIC EYES OF SEVEN PATIENTS*
Normal 1. 2. 3. 4. 5. 6. 7.
6/6 6/9 6/6 6/6 6/6 6/6 6/6
B
A
Visual Acuity
C
Amblyopic
Normal
Amblyopic
Normal
Amblyopic
Normal
Amblyopic
5/60 6/60 6/30 6/60 6/21 6/21 6/6f
20 20 9 17 16 9 28f
25 Central first 7 7 12 8 24t
29 37 38 >45 11 9 40 f
12 Central first 7 16 18 7 35 f
>55 >55 >45 55 40 11 >55f
17 11 9 35 33 11 >55f
* Targets were 1.7° in diameter and 5.7° apart. The red target was always temporal to the white and of lower intensity. In Column A are times in seconds for disappearance of red target when fixing on the white one. In Column B are times in seconds for disappearance of the white target while fixating the red one. In Column C are times m seconds for disappearance of the red target while fixing on it. t Normal patient.
functional amblyopia is, to at least some ex tent, reversible, or can be accentuated in the normal eye by occlusion. CONCLUSIONS
The experiments described here indicate that there is an accelerated local adaptation in the central and paracentral regions of the visual field of amblyopic eyes. Further, this local adaptation is related to the differences noted subjectively between amblyopic and normal eyes in the vision-testing situation. However, these experiments also indicate that this accelerated local adaptation is not solely responsible for the poor vision which can be measured in these eyes. In fact, to a limited degree the results of one of these ex periments indicate that the local adaptation may be completely unrelated to the poor vi sion. There is the possibility that adaptation in the amblyopic eye is potentiated by the al most constant state of supression in that eye, thus adding another facet to local adaptation. SUMMARY
Three experiments dealing with compari sons between amblyopic and normal eyes are described. The first demonstrated that the fixation pattern of amblyopic eyes differs from that of normal eyes. The timing of the different subjective phenomena noted in these eyes can be correlated with the timing of fix
ation events. In the second experiment it was not possible to demonstrate that as ex posure time of acuity targets is reduced when comparing amblyopic with normal eyes, the respective visual acuities of the two eyes tend to become similar. In the third experi ment it was demonstrated that local adapta tion proceeds faster in the central and para central region of the amblyopic eye than in the normal fellow eye. Department of Ophthalmology University of Louisville School of Medicine 323 Chestnut Street (20402) ACKNOWLEDGMENTS
I should like to thank Dr. Hermann Burian for the opportunity of working in his laboratory, and LTC Budd Appleton for his review of the paper. REFERENCES
1. Pugh, M.: Brightness perception and binocular adaptation. Brit. J. Ophth. 35:134, 1951. 2. Pugh, M.: Foveal vision in amblyopia. Brit. J. Ophth. 38:321, 1954. 3. Pugh, M.: Visual distortion in amblyopia. Brit. J. Ophth. 42 :449, 1958. 4. Lawwill, T.: The fixation pattern of the light-adapted and dark-adapted amblyopic eye. Am. J. Ophth. 61:1416, 1966. 5. Lawwill, T. and Burian, H. M.: Luminance, contrast function and visual acuity in functional amblyopia. Am. J. Ophth. 62:511, 1966. 6. Stuart, J. A. and Burian, H. M.: A study of separation difficulty: Its relationship to visual acuity in normal and amblyopic eyes. Am. J. Ophth. 53:471, 1962.