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Loss in Pattern-Elicited Electroretinograms in Optic Nerve Dysfunction
LOSS IN PATTERN-ELICITED ELECTRORETINOGRAMS IN OPTIC NERVE DYSFUNCTION JAMES G. MAY, P H . D . , JAMES V. RALSTON, M . S . , JANICE L. REED, B . S . , AND HENRY J . L. VAN DYK, M . D . New Orleans, Louisiana
Bothflash-and pattern-elicited electroretinograms and visual-evoked potentials were recorded from a patient with well-documented unilateral optic nerve dysfunction. Although theflash-elicitedelectroretinograms from the left and right eyes did not differ in amplitude or latency, theflash-elicitedvisual-evoked potentials were greatly attenuated. Prominent pattern-elicited electroretinograms and visual-evoked potentials were recorded from the better eye, but neither could be obtained from the affected eye. These results supported the contention that pattern-elicited electroretinograms are derived from optic nerve activity and that the absence of such responses may be diagnostic of loss of optic nerve function. This suggests that testing protocols aimed at assessing optic nerve function might benefit from the inclusion of pattern-elicited electroretinographic recordings. We also obtained contrast sensitivity functions from both eyes. Although considerably suppressed, the contrast sensitivity of the affected eye exhibited a 3-octave range, indicating some pattern-processing capability.
the work of Wachtmeister and Dowling indicated that the isopotential sites for all components are well within the inner nuclear layer, suggesting that these components do not emanate from the ganglion cells. Also, in vitro recordings from the retinas of rats and from human retinas indicated the presence of oscillatory potentials. Thus, it is generally accepted that flash-elicited electroretinographic components are generated peripheral to the ganglion cell somas or dendrites and that these recordings cannot be used to Accepted for publication Jan. 8, 1982. assess optic nerve integrity. From the Lions Eye Research Laboratories, LSU Eye Center, LSU Medical Center School of MediRecently, Maffei and Fiorentini recine, New Orleans, and the Department of Psycholoported that they were unable to record gy, University of New Orleans, New Orleans, Louisipattern-elicited electroretinograms in ana. This study was supported in part by grants EY03483 (Dr. May) and EY02377 from the National cats four months after optic nerve tranEye Institute. section although flash-elicited electroretReprint requests to James G. May, Ph.D., LSU Eye Center, 136 S. Roman St., New Orleans, LA inograms were essentially normal. Using 70112. a phase-reversal technique first em-
Early experiments with flash-elicited electroretinograms demonstrated that the amplitude and latency of the a- and b-waves are unaffected by optic nerve transection, and Granit and Helme showed that electrical stimulation of the optic nerve does not alter flash-elicited electroretinographic amplitude or latency. Although some investigators have speculated that the oscillatory potentials are derived from optic nerve discharge, 1
4
2
6
6
3
7
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©AMERICAN JOURNAL OF OPHTHALMOLOGY 93:418-422, 1982
VOL. 93, NO. 4
BITTERN-ELICITED ELECTRORETINOGRAMS
ployed by Riggs, Johnson, and Schick, Maffei and Fiorentini recorded electroretinograms before and at different times after optic nerve transection using, as stimuli, gratings at different spatial frequencies. They found that, in the course of optic nerve degeneration, responses to low spatial frequency gratings vanished first, while responses to higher spatial frequency gratings persisted for a longer period of time. We have recorded flash- and patternelicited electroretinograms and visualevoked potentials from a patient with unilateral optic nerve head compression secondary to glaucoma to ascertain if the results obtained by Maffei and Fiorentini in cats also occur in human subjects with optic nerve dysfunction. 8
CASE REPORT A 22-year-old man was first examined for blurring of vision in his right eye in December 1979. His visual acuity was R.E.: 6/12 (20/40) and L.E.: 6/6 (20/20). The intraocular pressure was R.E.: 29 mm Hg and L.E.: 15 mm Hg by applanation tonometry. Gonioscopy disclosed wide-open angles in both eyes. The optic disks had asymmetric cups with cup-disk ratios of R.E.: 0.7 and L.E. : 0.2 to 0.3. The visual fields, measured by Goldmann perimetry,
8
showed an extensive superior arcuate defect in the right eye but no defect in the left eye. Open-angle glaucoma was diagnosed and the patient began using 0.5% timolol maléate twice a day in his right eye. In September 1981, the patient returned because the vision in his left eye had become affected. He confessed that he had not had his prescription filled. His visual acuity was R.E.: hand motions and L.E.: 6/7.5 (20/25). The intraocular pressure was R.E.: 36 mm Hg and L.E.: 30 mm Hg by applanation tonometry. The right optic disk was atrophic and totally cupped, with a cup-disk ratio of 0.99; the left optic disk showed moderate cupping with a cup-disk ratio of 0.5 to 0.6 (Fig. 1). Repeat visual fields showed only a small inferior temporal crescent of vision remaining in the right eye. The left eye showed a moderate concentric contraction of all isopters with no arcuate defect or nasal step. There was a relative afferent pupillary defect in the right eye. Direct and indirect ophthalmoscopy disclosed normal retinal peripheries in both eyes. MATERIAL AND METHODS
Flash stimuli were produced with a ganzfeld stimulator equipped with a photostimulator. We used a high intensity (level eight) while the patient's eyes were closed. The stimulus repetition rates were 8 and 2 Hz. The patterned stimuli were displayed on a large-screen cathode ray tube. Checkerboard patterns were generated with a custom-built cathode ray tube con-
o ejp j
240
255
270
LEFT
285
300
419
240
2SS
270
285
300
RIGHT
Fig. 1 (May and associates). Visual fields obtained for the left and right eyes.
420
AMERICAN JOURNAL OF OPHTHALMOLOGY
troller and phase-alternated at a rate of 8 Hz. We used checks of three different sizes; their widths subtended 50, 42, or 23 minutes of visual angle. The patient viewed the screen from a distance of 2 m. Overall the screen subtended 12 degrees. During the recording of pattern-elicited responses, the patient's fixation was monitored by an experimenter to assure proper stimulation. Trigger pulses could be interrupted during periods of unwanted activity, thus excluding such responses from the summation. We recorded the electroretinograms and visual-evoked potentials simultaneously from each eye. The electroretino-
APRIL, 1982
grams were recorded with electrodes made of silver-impregnated nylon applied to the cornea, with a silver/silver chloride (Ag/AgCl) reference electrode affixed to the ipsilateral ear and an Ag/AgCl ground electrode affixed to the contralateral ear. The visual-evoked potentials were recorded with the active electrode 2.5 cm above the inion on the midline. The reference and ground electrodes were common to both recording channels. These bio-electric potentials were amplified (x 35,000) and filtered (1 to 30 Hz) with a two-channel amplifier before being recorded at a speed of 3.75 inches per second on two channels of a 9
Fig. 2 (May and associates). Electrophysiologic responses elicited at a stimulus rate of 8 Hz from the left (tracings at left) and right (tracings at right) eyes. Theflash-elicitedvisualevoked potential (FVEP) from the right eye was drastically reduced compared to the response from the left eye. The flash-elicited electroretinograms (FERG) from the two eyes had the same amplitudes and latencies. Prominent pattern-elicited visual-evoked responses (PVEP) and electroretinograms (PERG) were recorded at three different check widths from the left eye, but no such responses were observed after stimulation of the right eye.
2 9 6 nute
VOL. 93, NO. 4
PATTERN-ELICITED ELECTRORETINOGRAMS
tape recorder. Trigger pulses associated with each stimulus event were recorded on a third (direct) channel. We monitored the raw electroretinograms and visualevoked potentials with an oscilloscope during recording. We excluded trials marred by excessive eye blinks or muscle artifacts. All responses were summed offline with a signal averager. The summation of the flash electroretinograms and visual-evoked potentials was based on 64 sweeps. The summation of patternelicited responses was based on 256 stimulus presentations. Contrast sensitivity measurements were obtained for each eye with the same apparatus. We used sine-wave gratings of 0.5, 1, 2, 4, 8, and 16 cycles per degree (cpd). The experimenter varied the contrast according to a modified staircase method of limits, and the patient indicated whether or not he could see the grating at each setting. RESULTS
The flash-elicited electroretinograms from both eyes were similar in amplitude and latency (Fig. 2). The flash-elicited visual-evoked potentials obtained from the right eye were reduced by 85% compared to those recorded from the left eye. Prominent pattern-elicited electroretinograms and visual-evoked potentials were recorded from the left eye at all check sizes, but no reliable waveforms were elicited from the right eye with any pattern stimulus. Stimulation at 8 and 2 Hz produced similar results. No pattern-elicited responses could be obtained from the right eye. When the left eye was stimulated at high spatial frequencies, contrast sensitivity was somewhat reduced compared to the normal findings in our laboratory, while the right eye exhibited a drastic loss of contrast sensitivity at all spatial frequencies (Fig. 3). However, at very
421
high contrasts, the right eye was sensitive to a 3-octave range of spatial frequencies in the low to medium region. DISCUSSION
The absence of pattern-elicited responses in a human eye with known optic nerve dysfunction suggests that, in man as in the cat, the pattern-elicited electroretinogram is derived from optic nerve activity. If this is true, clinical protocols using such responses may prove valuable in the assessment of optic nerve function in glaucoma and in other disorders such as optic neuritis and amblyopia. Visualevoked potentials are altered by all of these disorders, but pattern-elicited electroretinograms have been only recently investigated in patients with macular disease, amblyopia, and optic nerve disease. We were also interested in the degree of perceptual processing possible with the severely restricted visual field in the 1011
12
13
1000 i
0.5
1.0
2.0
4.0
8.0
16.0
32.0
SPATIAL FREQUENCY (C/D)
Fig. 3 (May and associates). Contrast sensitivity as a function of spatial frequency of a vertical sine-wave grating for the left andrighteyes (solid curves). The dashed line represents the average contrast sensitivity for six normal observers.
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AMERICAN JOURNAL OF OPHTHALMOLOGY
patient's right eye. Ginsburg described a patient with a coloboma that disrupted all but a small peripheral portion of her visual field. This patient was able to recognize faces, read print, and ride a bicycle. Ginsburg determined that the minimum contrast sensitivity needed for most pattern recognition was a range of at least 2 octaves. He suggested that a considerable amount of functional pattern processing is possible if the contrast sensitivity spans this range, even if the visual field is small. Our patient could see only 1 cycle of the grating at 0.5 cpd, but he was able to detect a grating (at high contrast) at up to 4 cpd. When he held large, well-lighted, high-contrast print close enough, he could read in a cumbersome fashion. This relationship between functional vision and contrast sensitivity is of some importance for patients with poor visual acuities. In summary, these findings indicated that pattern-elicited electroretinograms offer information regarding optic nerve function where flash-elicited electroretinograms or visual-evoked potentials may not. Additionally, we found that a patient whose optic nerve had been severely compromised and who was described as capable of seeing only hand motions with his affected eye was still able to carry out sophisticated pattern perception when the viewing conditions were tailored to his constrained visual field and contrast was increased. We plan to extend our use of such testing to other patients with optic nerve problems. 14
APRIL, 1982
REFERENCES 1. Noell, W.: Studies on the electrophysiology and metabolism of the retina. Project No. 211201-0004, Report No. 1. Randolph Field, Texas, United States Air Force School of Aviation Medicine, 1953. 2. Granit, R., and Helme, L. : Changes in retinal excitability due to polarization and some observations on the relation between the processes in retina and nerve. J. Neurophysiol. 2:556, 1939. 3. Fry, G. A., and Bartley, S. H.: Electrical response of the ganglion cell axons. J. Cell. Comp. Physiol. 5:291, 1934-1935. 4. Wachtmeister, L., and Dowling, I. E.: The oscillatory potentials of the mudpuppy retina. Invest. Ophthalmol. Vis. Sei. 17:1176, 1978. 5. Winkler, B. S.: The electro re tinogram of the isolated rat retina. Vision Res. 12:1183, 1972. 6. Honda, Y., and Nagata, M.: Electrical activity of the human retina in vitro. Am. J. Ophthalmol. 68:925, 1969. 7. Maffei, L., and Fiorentini, A.: Electroretuiographic responses to alternating gratings before and after section of the optic nerve. Science 211:953, 1981. 8. Riggs, L. A., Johnson, E. P., and Schick, A. M.: Electrical responses of the human eye to moving stimulus patterns. Science 144:567, 1964. 9. Dawson, W. W., Trick, G. L., and Litzkow, C. A.: Improved electroretinography. Invest. Ophthalmol. Vis. Sei. 18:988, 1979. 10. Lawwill, T.: The bar-pattern electroretinogram for clinical evaluation of the central retina. Am. J. Ophthalmol. 78:121, 1974. 11. Sokol, S., and Bloom, B. H.: Macular ERGs elicited by checkerboard pattern stimuli. Doc. Ophthalmol. 13:299, 1977. 12. Sokol, S., and Nadler, D.: Simultaneous electroretinograms and visually evoked potentials from adult amblyopes in response to a pattern stimulus. Invest. Ophthalmol. Vis. Sei. 18:848, 1979. 13. Fiorentini, A., Maffei, L., Pirchio, M., Spinelli, D., and Porcellati, V.: The ERG in response to alternating gratings in patients with diseases of the peripheral visual pathway. Invest. Ophthalmol. Vis. Sei. 21:490, 1981. 14. Ginsburg, A. : Spatialfilteringin vision. Duplications for normal and abnormal vision. In Proenza, L., Enoch, J., and Jampolsky, A. (eds. ): Applications of Psychophysics to Clinical Problems. London, Cambridge University Press, 1981, pp. 70-106.
Bothflash-and pattern-elicited electroretinograms and visual-evoked potentials were recorded from a patient with well-documented unilateral optic nerve dysfunction. Although theflash-elicitedelectroretinograms from the left and right eyes did not differ in amplitude or latency, theflash-elicitedvisual-evoked potentials were greatly attenuated. Prominent pattern-elicited electroretinograms and visual-evoked potentials were recorded from the better eye, but neither could be obtained from the affected eye. These results supported the contention that pattern-elicited electroretinograms are derived from optic nerve activity and that the absence of such responses may be diagnostic of loss of optic nerve function. This suggests that testing protocols aimed at assessing optic nerve function might benefit from the inclusion of pattern-elicited electroretinographic recordings. We also obtained contrast sensitivity functions from both eyes. Although considerably suppressed, the contrast sensitivity of the affected eye exhibited a 3-octave range, indicating some pattern-processing capability.
the work of Wachtmeister and Dowling indicated that the isopotential sites for all components are well within the inner nuclear layer, suggesting that these components do not emanate from the ganglion cells. Also, in vitro recordings from the retinas of rats and from human retinas indicated the presence of oscillatory potentials. Thus, it is generally accepted that flash-elicited electroretinographic components are generated peripheral to the ganglion cell somas or dendrites and that these recordings cannot be used to Accepted for publication Jan. 8, 1982. assess optic nerve integrity. From the Lions Eye Research Laboratories, LSU Eye Center, LSU Medical Center School of MediRecently, Maffei and Fiorentini recine, New Orleans, and the Department of Psycholoported that they were unable to record gy, University of New Orleans, New Orleans, Louisipattern-elicited electroretinograms in ana. This study was supported in part by grants EY03483 (Dr. May) and EY02377 from the National cats four months after optic nerve tranEye Institute. section although flash-elicited electroretReprint requests to James G. May, Ph.D., LSU Eye Center, 136 S. Roman St., New Orleans, LA inograms were essentially normal. Using 70112. a phase-reversal technique first em-
Early experiments with flash-elicited electroretinograms demonstrated that the amplitude and latency of the a- and b-waves are unaffected by optic nerve transection, and Granit and Helme showed that electrical stimulation of the optic nerve does not alter flash-elicited electroretinographic amplitude or latency. Although some investigators have speculated that the oscillatory potentials are derived from optic nerve discharge, 1
4
2
6
6
3
7
418
©AMERICAN JOURNAL OF OPHTHALMOLOGY 93:418-422, 1982
VOL. 93, NO. 4
BITTERN-ELICITED ELECTRORETINOGRAMS
ployed by Riggs, Johnson, and Schick, Maffei and Fiorentini recorded electroretinograms before and at different times after optic nerve transection using, as stimuli, gratings at different spatial frequencies. They found that, in the course of optic nerve degeneration, responses to low spatial frequency gratings vanished first, while responses to higher spatial frequency gratings persisted for a longer period of time. We have recorded flash- and patternelicited electroretinograms and visualevoked potentials from a patient with unilateral optic nerve head compression secondary to glaucoma to ascertain if the results obtained by Maffei and Fiorentini in cats also occur in human subjects with optic nerve dysfunction. 8
CASE REPORT A 22-year-old man was first examined for blurring of vision in his right eye in December 1979. His visual acuity was R.E.: 6/12 (20/40) and L.E.: 6/6 (20/20). The intraocular pressure was R.E.: 29 mm Hg and L.E.: 15 mm Hg by applanation tonometry. Gonioscopy disclosed wide-open angles in both eyes. The optic disks had asymmetric cups with cup-disk ratios of R.E.: 0.7 and L.E. : 0.2 to 0.3. The visual fields, measured by Goldmann perimetry,
8
showed an extensive superior arcuate defect in the right eye but no defect in the left eye. Open-angle glaucoma was diagnosed and the patient began using 0.5% timolol maléate twice a day in his right eye. In September 1981, the patient returned because the vision in his left eye had become affected. He confessed that he had not had his prescription filled. His visual acuity was R.E.: hand motions and L.E.: 6/7.5 (20/25). The intraocular pressure was R.E.: 36 mm Hg and L.E.: 30 mm Hg by applanation tonometry. The right optic disk was atrophic and totally cupped, with a cup-disk ratio of 0.99; the left optic disk showed moderate cupping with a cup-disk ratio of 0.5 to 0.6 (Fig. 1). Repeat visual fields showed only a small inferior temporal crescent of vision remaining in the right eye. The left eye showed a moderate concentric contraction of all isopters with no arcuate defect or nasal step. There was a relative afferent pupillary defect in the right eye. Direct and indirect ophthalmoscopy disclosed normal retinal peripheries in both eyes. MATERIAL AND METHODS
Flash stimuli were produced with a ganzfeld stimulator equipped with a photostimulator. We used a high intensity (level eight) while the patient's eyes were closed. The stimulus repetition rates were 8 and 2 Hz. The patterned stimuli were displayed on a large-screen cathode ray tube. Checkerboard patterns were generated with a custom-built cathode ray tube con-
o ejp j
240
255
270
LEFT
285
300
419
240
2SS
270
285
300
RIGHT
Fig. 1 (May and associates). Visual fields obtained for the left and right eyes.
420
AMERICAN JOURNAL OF OPHTHALMOLOGY
troller and phase-alternated at a rate of 8 Hz. We used checks of three different sizes; their widths subtended 50, 42, or 23 minutes of visual angle. The patient viewed the screen from a distance of 2 m. Overall the screen subtended 12 degrees. During the recording of pattern-elicited responses, the patient's fixation was monitored by an experimenter to assure proper stimulation. Trigger pulses could be interrupted during periods of unwanted activity, thus excluding such responses from the summation. We recorded the electroretinograms and visual-evoked potentials simultaneously from each eye. The electroretino-
APRIL, 1982
grams were recorded with electrodes made of silver-impregnated nylon applied to the cornea, with a silver/silver chloride (Ag/AgCl) reference electrode affixed to the ipsilateral ear and an Ag/AgCl ground electrode affixed to the contralateral ear. The visual-evoked potentials were recorded with the active electrode 2.5 cm above the inion on the midline. The reference and ground electrodes were common to both recording channels. These bio-electric potentials were amplified (x 35,000) and filtered (1 to 30 Hz) with a two-channel amplifier before being recorded at a speed of 3.75 inches per second on two channels of a 9
Fig. 2 (May and associates). Electrophysiologic responses elicited at a stimulus rate of 8 Hz from the left (tracings at left) and right (tracings at right) eyes. Theflash-elicitedvisualevoked potential (FVEP) from the right eye was drastically reduced compared to the response from the left eye. The flash-elicited electroretinograms (FERG) from the two eyes had the same amplitudes and latencies. Prominent pattern-elicited visual-evoked responses (PVEP) and electroretinograms (PERG) were recorded at three different check widths from the left eye, but no such responses were observed after stimulation of the right eye.
2 9 6 nute
VOL. 93, NO. 4
PATTERN-ELICITED ELECTRORETINOGRAMS
tape recorder. Trigger pulses associated with each stimulus event were recorded on a third (direct) channel. We monitored the raw electroretinograms and visualevoked potentials with an oscilloscope during recording. We excluded trials marred by excessive eye blinks or muscle artifacts. All responses were summed offline with a signal averager. The summation of the flash electroretinograms and visual-evoked potentials was based on 64 sweeps. The summation of patternelicited responses was based on 256 stimulus presentations. Contrast sensitivity measurements were obtained for each eye with the same apparatus. We used sine-wave gratings of 0.5, 1, 2, 4, 8, and 16 cycles per degree (cpd). The experimenter varied the contrast according to a modified staircase method of limits, and the patient indicated whether or not he could see the grating at each setting. RESULTS
The flash-elicited electroretinograms from both eyes were similar in amplitude and latency (Fig. 2). The flash-elicited visual-evoked potentials obtained from the right eye were reduced by 85% compared to those recorded from the left eye. Prominent pattern-elicited electroretinograms and visual-evoked potentials were recorded from the left eye at all check sizes, but no reliable waveforms were elicited from the right eye with any pattern stimulus. Stimulation at 8 and 2 Hz produced similar results. No pattern-elicited responses could be obtained from the right eye. When the left eye was stimulated at high spatial frequencies, contrast sensitivity was somewhat reduced compared to the normal findings in our laboratory, while the right eye exhibited a drastic loss of contrast sensitivity at all spatial frequencies (Fig. 3). However, at very
421
high contrasts, the right eye was sensitive to a 3-octave range of spatial frequencies in the low to medium region. DISCUSSION
The absence of pattern-elicited responses in a human eye with known optic nerve dysfunction suggests that, in man as in the cat, the pattern-elicited electroretinogram is derived from optic nerve activity. If this is true, clinical protocols using such responses may prove valuable in the assessment of optic nerve function in glaucoma and in other disorders such as optic neuritis and amblyopia. Visualevoked potentials are altered by all of these disorders, but pattern-elicited electroretinograms have been only recently investigated in patients with macular disease, amblyopia, and optic nerve disease. We were also interested in the degree of perceptual processing possible with the severely restricted visual field in the 1011
12
13
1000 i
0.5
1.0
2.0
4.0
8.0
16.0
32.0
SPATIAL FREQUENCY (C/D)
Fig. 3 (May and associates). Contrast sensitivity as a function of spatial frequency of a vertical sine-wave grating for the left andrighteyes (solid curves). The dashed line represents the average contrast sensitivity for six normal observers.
422
AMERICAN JOURNAL OF OPHTHALMOLOGY
patient's right eye. Ginsburg described a patient with a coloboma that disrupted all but a small peripheral portion of her visual field. This patient was able to recognize faces, read print, and ride a bicycle. Ginsburg determined that the minimum contrast sensitivity needed for most pattern recognition was a range of at least 2 octaves. He suggested that a considerable amount of functional pattern processing is possible if the contrast sensitivity spans this range, even if the visual field is small. Our patient could see only 1 cycle of the grating at 0.5 cpd, but he was able to detect a grating (at high contrast) at up to 4 cpd. When he held large, well-lighted, high-contrast print close enough, he could read in a cumbersome fashion. This relationship between functional vision and contrast sensitivity is of some importance for patients with poor visual acuities. In summary, these findings indicated that pattern-elicited electroretinograms offer information regarding optic nerve function where flash-elicited electroretinograms or visual-evoked potentials may not. Additionally, we found that a patient whose optic nerve had been severely compromised and who was described as capable of seeing only hand motions with his affected eye was still able to carry out sophisticated pattern perception when the viewing conditions were tailored to his constrained visual field and contrast was increased. We plan to extend our use of such testing to other patients with optic nerve problems. 14
APRIL, 1982
REFERENCES 1. Noell, W.: Studies on the electrophysiology and metabolism of the retina. Project No. 211201-0004, Report No. 1. Randolph Field, Texas, United States Air Force School of Aviation Medicine, 1953. 2. Granit, R., and Helme, L. : Changes in retinal excitability due to polarization and some observations on the relation between the processes in retina and nerve. J. Neurophysiol. 2:556, 1939. 3. Fry, G. A., and Bartley, S. H.: Electrical response of the ganglion cell axons. J. Cell. Comp. Physiol. 5:291, 1934-1935. 4. Wachtmeister, L., and Dowling, I. E.: The oscillatory potentials of the mudpuppy retina. Invest. Ophthalmol. Vis. Sei. 17:1176, 1978. 5. Winkler, B. S.: The electro re tinogram of the isolated rat retina. Vision Res. 12:1183, 1972. 6. Honda, Y., and Nagata, M.: Electrical activity of the human retina in vitro. Am. J. Ophthalmol. 68:925, 1969. 7. Maffei, L., and Fiorentini, A.: Electroretuiographic responses to alternating gratings before and after section of the optic nerve. Science 211:953, 1981. 8. Riggs, L. A., Johnson, E. P., and Schick, A. M.: Electrical responses of the human eye to moving stimulus patterns. Science 144:567, 1964. 9. Dawson, W. W., Trick, G. L., and Litzkow, C. A.: Improved electroretinography. Invest. Ophthalmol. Vis. Sei. 18:988, 1979. 10. Lawwill, T.: The bar-pattern electroretinogram for clinical evaluation of the central retina. Am. J. Ophthalmol. 78:121, 1974. 11. Sokol, S., and Bloom, B. H.: Macular ERGs elicited by checkerboard pattern stimuli. Doc. Ophthalmol. 13:299, 1977. 12. Sokol, S., and Nadler, D.: Simultaneous electroretinograms and visually evoked potentials from adult amblyopes in response to a pattern stimulus. Invest. Ophthalmol. Vis. Sei. 18:848, 1979. 13. Fiorentini, A., Maffei, L., Pirchio, M., Spinelli, D., and Porcellati, V.: The ERG in response to alternating gratings in patients with diseases of the peripheral visual pathway. Invest. Ophthalmol. Vis. Sei. 21:490, 1981. 14. Ginsburg, A. : Spatialfilteringin vision. Duplications for normal and abnormal vision. In Proenza, L., Enoch, J., and Jampolsky, A. (eds. ): Applications of Psychophysics to Clinical Problems. London, Cambridge University Press, 1981, pp. 70-106.