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Show Journal of Neuro- Ophthalmology 16( 1): 36- 40, 1996. © 1996 Lippincott- Raven Publishers, Philadelphia Pulfrich Psychophysical Stereo- Illusion and Visual- Evoked Potentials in Epiretinal Membrane of the Macula Albert J. Hofeldt, M. D., Gregory T. Hofeldt, B. SC, and Michael J. Weiss, M. D., Ph. D. Six patients with unilateral epiretinal membrane of the macula perceived the spontaneous Pulfrich psychophysical stereo- illusion, suggesting a relative conduction delay on the side of the membrane. In three of these patients, visual- evoked potential studies were also obtained and confirmed an absolute conduction delay in the anterior pathway on the side of the epiretinal membrane in two patients and an absence of the P 100 wave on the side of the epiretinal membrane in the third patient. It is important to recognize that the Pulfrich psychophysical stereo- illusion can be spontaneously perceived in macula disease, and therefore, the test may not always distinguish optic nerve from macula disease. Key Words: Epiretinal membrane- Pulfrich stereo-illusion- Visual- evoked potentials- Optic nerve. The spontaneous Pulfrich psychophysical stereo- illusion is generally viewed as a simple, inexpensive, and sensitive test of optic nerve dysfunction ( 1- 4). We describe six patients with unilateral epiretinal membrane of the macula, without demonstrable optic nerve disease, who perceived the spontaneous Pulfrich stereo- illusion response. In three of these patients, pattern shift visual- evoked potentials were also obtained to confirm objectively a conduction delay in the anterior visual pathway. METHODS AND MATERIALS A real pendulum device ( Patent Number 5,099,858) or a video of the computer- generated image was used in testing the Pulfrich psychophysical stereo- illusion. If the pendulum appeared to move in an orbit around the cone, we classified the response as spontaneous and had the subject specify the direction as clockwise ( conduction delay LE) or counterclockwise ( conduction delay RE) rotation. If the initial response was spontaneous, graded neutral density ( ND) filters in 0.10- ND increments were placed in front of the eye opposite the defect to neutralize the psychophysical stereo-illusion. If the initial response was not spontaneous, filters of increasing density were placed in front of one eye at a time to induce the Pulfrich psychophysical stereo- illusion. From the Edward S. Harkness Eye Institute, Columbia University, New York, New York, U. S. A. Address correspondence and reprint requests to Dr. A. J. Hofeldt, 945 Lexington Avenue, New York, NY 10021, U. S. A. CASE REPORTS Case 1 A 61- year- old man with diabetes mellitus but without and diabetic retinopathy experienced an acute posterior vitreous detachment LE, compli- 36 EPIRETINAL MEMBRANE OF THE MACULA 37 cated by the development of a small horseshoe tear in the superotemporal quadrant of that eye. The tear was successfully treated with transconjunctival retinal cryopexy. Six years later, he returned with symptoms of floaters RE of 3 months' duration. His acuity measured 20/ 30 in each eye. The Amsler grid appeared distorted centrally RE but not LE. Color- vision testing was normal in both eyes, as tested with the American Optical pseudoisochromatic color plates. The pupils were equal, and there was no relative afferent pupillary defect. The Pulfrich psychophysical stereo- illusion was spontaneous in the counterclockwise rotation and could be neutralized by placing a 0.30 ND filter in front of LE. There was a mild and equal degree of lenticular nuclear sclerosis in each eye. Vitreoreti-nal examination was notable for a detached posterior hyaloid in both eyes and an epiretinal membrane of the macula RE. The optic nerves appeared normal in both eyes. Case 2 A 58- year- old man who was first seen with a rhegmatogenous retinal detachment in the superotemporal quadrant RE. On visual field examination, a relative inferonasal scotoma reached 15° from fixation. His acuity measured 20/ 20 in each eye. The pupils were equal, and there was no relative afferent pupillary defect. The retina was successfully repaired with a local scleral buckle and cryopexy. The macula was never detached. Six weeks postoperatively, the vision was correctable to 20/ 20 in each eye. The Pulfrich psychophysical stereo- illusion was normal with induction by a 0.40 ND filter placed in front of either eye. At 3 months postoperatively, central distortion began RE, and the acuity declined to 20/ 30 RE. The pupils remained equal in size, and there was no relative afferent pupillary defect. American Optical color plate testing was normal in both eyes. Vit-reoretinal examination was remarkable for a fine epiretinal membrane of the macula RE. Both optic nerves appeared normal. A fluorescein angiogram RE disclosed a faint amount of dry leakage in the superior parafoveal area in the late- phase photographs ( Fig. 1) consistent with mild macula edema. A 1- month course of prednisone was prescribed at 60 mg/ day for 1 week followed by 40 mg every other day for 3 weeks. The distortion lessened, and the vision improved to 20/ 25 RE. Pulfrich psychophysical stereo- illusion test results changed compared to measurements obtained 6 weeks postoperatively and now demonstrated an abnormal spontaneous response in the counterclockwise FIG. 1. Case 2. In the late stage of fluorescein angiography, RE dye leakage is found in the superior and superotemporal parafoveal region, consistent with mild macula edema. direction and could be neutralized by a 0.30 ND filter placed over LE. Case 3 A 44- year- old man had a rhegmatogenous retinal detachment LE extending from the 2: 00 to 7: 00 meridians with the macula partially detached. His vision measured 20/ 15 RE and 20/ 50 LE. Visual field testing was normal RE and showed a loss of the nasal hemifield LE. A relative afferent pupillary defect was present LE. A scleral buckling procedure successfully reattached the retina. One year postoperatively, the vision measured 20/ 25 LE. Color vision was normal in both eyes as tested with the American Optical pseudoisochromatic plates. Central distortion was reported on Amsler grid testing LE. The pupils were equal, and there was no residual of the relative afferent pupillary defect found preoperatively. Biomicroscopic fundus examination found a normal macula RE and disclosed a fine epiretinal membrane over the left macula, which resulted in increased tortuosity of the retinal vessel inferior to the fovea. The optic disks appeared normal in both eyes. The Pulfrich psychophysical stereo- illusion was seen spontaneously rotating in a clockwise direction and could be neutralized by placing a 0.40- ND filter in front of RE. Case 4 A 61- year- old woman in good health reported distortion in the central vision RE. Her acuity mea- J Neuro- Ophthalmol, Vol. 16, No. 1, 1996 38 A. ]. HOFELDT ET AL. sured 20/ 70 RE and 20/ 25 LE. Color vision testing with American Optical color plates was normal in both eyes. The pupils were equal, and there was no relative afferent pupillary defect detected. Vit-reoretinal examination revealed a vitreous separation in both eyes and an epiretinal membrane of the macula RE. The optic disk appeared normal in both eyes. The Pulfrich psychophysical stereo-illusion was abnormal with a spontaneous response in the counterclockwise direction and could be neutralized with a 0.30- ND filter in front of LE. During a period of 3 years, the acuity declined to 20/ 100 RE, the distortion recorded on Am-sler grid increased, and the Pulfrich psychophysical stereo- illusion test remained abnormal. A fluorescein angiogram demonstrated tortuous and displaced vessels in the right macula, but no dye leakage was present in the macula at 30 min postinjection ( Fig. 2). The PI00 peak of the pattern shift reversal visual- evoked potential for large checks ( e. g., 47 min of arc) measured RE 130 ms and LE 110 ms. Case 5 A 44- year- old man had reduced acuity and central visual distortion in his right eye. Vision measured 20/ 25 RE and 20/ 20 LE. The Amsler grid appeared distorted when viewed with the RE but not LE. Visual field testing with the Goldmann perimeter was normal in both eyes. Color- vision testing with the American Optical pseudoisochromatic plates was normal in both eyes. The pupils were equal, and there was no afferent pupillary defect. In the RE, fundus examination revealed a posterior vitreous detachment, normal- appearing optic nerve head, and a prominent epiretinal membrane covering the macula. Fundus examination in the LE was unremarkable. A fluorescein angiogram of the RE showed an increase in vascular tortuosity in the region of the epiretinal membrane, but there was no dye leakage in any portion of the study, including the late 30- min postinjection photographs ( Fig. 3). The Pulfrich psychophysical stereo- illusion was seen spontaneously rotating in a counterclockwise direction and was neutralized by a 0.60- ND filter placed in front of the LE. Pattern shift reversal visual- evoked potential P100 latencies were 120 ms in the RE and 105 ms in the LE, using 24- min check size stimulus and 115 ms in the RE and 100 ms in the LE, using 47- min check size stimulus. Case 6 A 52- year- old woman became aware of visual distortion in her right eye 2 months after the onset FIG. 2. Case 4. Late- stage fluorescein angiogram of the RE demonstrating tortuous and displaced vessels in the right macula region without any dye leakage present. of floaters in that eye. Vision measured 20/ 20 in each eye. The Amsler grid appeared distorted to her RE. A Humphrey macula threshold visual field disclosed 5, 13, 19, and 25 decibels defects in the four quadrants closest to fixation in the RE, compared to a 0- decibel defect in the macula of the LE. Color- vision testing with American Optical color plates was normal in both eyes. The pupils were equal, and there was no relative afferent pupillary defect. In the RE, the posterior vitreous was separated, and a fine epiretinal membrane covered the macula. Both optic discs and the left macula appeared normal. A fluorescein angiogram RE showed no dye leakage in any portion of the study including the late 30- min postinjection photographs. The Pulfrich psychophysical stereo-illusion was seen as spontaneous and could be neutralized with a 1.0- ND filter in front of the LE. The pattern shift reversal visual- evoked potentials using small checks of 24 min produced a normal PI 00 latency of 95 ms in the LE and a virtual absence of the P100 wave in the RE. Larger checks of 47 min were not used during the testing. DISCUSSION The basis of the Pulfrich psychophysical stereo-illusion is thought to be a delay in the retinocortical conduction time ( visual latency) of the nerve im- / Neuro- Ophthalmol, Vol. 16, No. 1, 1996 EPIRETINAL MEMBRANE OF THE MACULA 39 FIG. 3. Case 5. Late- stage fluorescein angiogram of the RE, demonstrating increased vascular tortuosity in the region of the epiretinal membrane without any dye leakage. pulses along one side of the visual system. The difference in visual latency between the two eyes is interpreted as a disparity in space with a resultant stereo- illusion. The Pulfrich stereo- illusion can be artificially induced by placing an ND filter over one eye, suggesting that retinocortical conduction time takes longer for a dim image compared to a bright image. An inability to induce artificially the Pulfrich stereo- illusion by this method suggests defective stereopsis or difficulties in motion perception ( 5,6). A spontaneous Pulfrich stereo- illusion has been described predominantly in optic nerve disease, particularly demyelinating optic neuropathy ( 1- 4). The Pulfrich phenomenon has therefore been thought to be an inexpensive, simple, and sensitive method to differentiate optic nerve from macula disease. However, there are other conditions not related to optic nerve disease that may produce a spontaneous Pulfrich stereo- illusion Anisocoria, corneal opacities, and cataracts ( which may result in unequal retinal illumination) can produce a spontaneous Pulfrich stereo- illusion ( 6). In a previous report, we described four patients perceiving the spontaneous Pulfrich stereo- illusion with serous detachment of the macula secondary to central serous chorioretinopathy and senile macula degeneration ( 7). We now present six patients with unilateral epiretinal membrane of the macula perceiving the spontaneous Pulfrich psychophysical stereo- illusion. Within the limits of sensitivity of clinical testing, these patients had no demonstrable optic nerve disease, as evidenced by the absence of an afferent pupillary defect, normal color plate testing, and normal- appearing optic nerves. Pattern shift reversal visual- evoked potentials were also obtained in three patients to confirm objectively a delay in the visual latency. Attenuated amplitudes and decreased visual latencies as measured by pattern shift visual- evoked potentials in optic nerve and macula disease have been well documented ( 8- 18). In two patients, prolongation of the P100 was documented, and in a third patient, the P100 amplitude was diminished to a degree that rendered the wave unidentifiable when tested with 27- min size checks. The mechanism of visual delay in epiretinal membrane of the macula as measured subjectively by a spontaneous Pulfrich stereo- illusion and objectively by visual- evoked potentials is not clear. Image blur attenuates the amplitude of checkerboard patterns ( 19- 21) of the visual- evoked potential, and this has been suggested as the reason for the amplitude changes observed in epiretinal membranes ( 18). The latency of the visual- evoked potential using large checkerboard stimulus ( e. g., 50 min of arc) is not affected by image blur ( 19), whereas the latency of response to checkerboards made up of much smaller checks ( e. g., 12 min) is sensitive to changes in the refractive error ( 21). The effect of blur on latency occurs with both check and grating patterns, and the effect is greater the higher the spatial frequency ( 22). In case 4, the visual- evoked potential using large checks showed an abnormal delay on the side of the epiretinal membrane. Thus image blur alone cannot explain the prolonged latency. Macula edema, which occurs in 21% of cases having epiretinal membrane of the macula ( 23), is a possible explanation in case 2 for a prolonged visual latency. However, macula edema cannot be solely responsible, because cases 4, 5, and 6 had prolonged visual latencies and no evidence of dye leakage in the macula on fluorescein angiography. Other possible contributing factors to the visual delay are the light- attenuation effect of the epiretinal membrane and the pathophysiologic changes imposed on the retinal neurosensory elements from the fractional forces exerted by the membrane. It is important to recognize that the Pulfrich psychophysical stereo- illusion, like the visual- evoked potential, can be abnormal in macula diseases, as previously reported in serous sensory retinal detachment of the macula ( 14) and in this report, in epiretinal membrane of the macula. The Pulfrich / Neuro- Ophthalmol, Vol. 16, No. 1, 1996 40 A. J. HOFELDT ET AL. psychophysical stereo- illusion is a powerful diagnostic test, but the test does not reliably distinguish optic nerve from macula disease. REFERENCES 1. Grimsdale H. A note on Pulfrich's phenomenon with a suggestion on its possible clinical importance. Br J Ophthalmol 1925; 9: 63- 5. 2. Frisen L, Hoyt WF, Bird AC, Weale RA. Diagnostic uses of the Pulfrich phenomenon. Lancet 1973; 2: 385- 6. 3. Rushton D. Use of the Pulfrich pendulum for detecting abnormal delay in the visual pathway in multiple sclerosis. Brain 1975; 98: 283- 95. 4. Bishara S, Zelikowittch A. Pulfrichs phenomenon and drusen of the optic nerve head. Ann Ophthalmol 1984; 16: 27- 9. 5. Pulfrich C. Die Stereoskopic in Dienste der isochromen und heterochromen Photometrie. Naturwissenschaften 1922; 10: 553- 64, 569- 74, 598- 601, 714- 22, 735^ 3, 751- 61. 6. Sokol S. The Pulfrich stereo- illusion as an index of optic nerve dysfunction. Surv Ophthalmol 1976; 20( 6): 432- 4. 7. Hofeldt AJ, Leavitt J, Behrens MM. Pulfrich stereo- illusion phenomenon in serous sensory retinal detachment of the macula. Am ] Ophthalmol 1985; 100: 576- 80. 8. Halliday AM, Mcdonald WI, Mushin J. Delayed pattern-evoked responses in optic neuritis. Lancet 1972; 1: 982- 5. 9. Halliday AM, Halliday E, Kriss A, Mcdonald WI, Mushin J. The pattern- evoked potential in compression of the anterior visual pathways. Brain 1976; 99: 357- 4. 10. Wist ER, Hennerici M, Dichgans J. The Pulfrich spatial frequency phenomenon: a psychophysical method competitive to visual evoked potentials in the diagnosis of multiple sclerosis. / Neurol Neurosurg Psychiatry 1978; 41: 1069- 77. 11. Scholl GB, Song H, Winkler DE, Wray SH. The pattern visual evoked potential and pattern electroretinogram in drusen- associated optic neuropathy. Arch Ophthalmol 1992; 110: 75- 81. 12. Greenberg HS. Visual- evoked resposes. / Clin Neuro Ophthalmol 1981; 1: 273- 5. 13. Lennerstrand G. Delayed visual evoked cortical potentials in retinal disease. Acta Ophthalmol 1982; 60: 497- 504. 14. Marcus M, Merin S, Wolf M, Feinsod M. Electrophysiologic tests in assessment of senile macula degeneration. Ann Ophthalmol 1983; 15: 235- 8. 15. Papakostopoulos D, Hart CD, Cooper R, Natsikos V. Combined electrophysiological assessment of the visual system in central serous retinopathy. Electroencephalogr Clin Neuro-physiol 1984; 59: 77- 80. 16. Bass SJ, Sherman J, Bodis- Wollner I, Nath S. Visual- evoked potentials in macular disease. Invest Ophthalmol Vis Sci 1971; 26: 1071- 1. 17. Johnson LN, Yee RD, Hepler RS, Martin DA. Alteration of the visual- evoked potential by macular holes: comparison with optic neuritis. Graefes Arch Clin Exp Ophthalmol 1987; 225: 123- 8. 18. Mehta MC, Katsume O, Buzney SM, Hirose T. Pattern reversal visual- evoked response as a prognostic indicator in macular gliosis. Am ] Ophthalmol 1992; 113: 39- 44. 19. Halliday AM, Mushin J. The visual evoked potential in neuro- ophthalmology. In: Sokol S, ed. Electrophysiology and psychophysics: their use in ophthalmic diagnosis. Int Ophthalmol Clin 1980; 20: 155- 183. 20. Katsumi O, Hirose T, Hiroshi S, Mehta M, Rosenstein RB. Effect of optical defocus on the steady state pattern reversal visual- evoked response. Ophthalmic Res 1990; 22: 383- 90. 21. Collins DWK, Carroll WM, Black JL, Walsh M. Effect of refractive error on the visual evoked response. Br Med } 1979; 1: 231- 2. 22. Bobak P, Wollner L, Guillory S. The effect of blur and contrast on VEP latency: comparison between check and sinusoidal grating patterns. Electroencephalogr Clin Neurophysiol 1987; 68: 247- 55. 23. Sidd RJ, Fine LF, Owens SL, Patz A. Idiopathic preretinal gliosis. Am ] Ophthalmol 1982; 94: 44- 8. / Neuro- Ophthalmol, Vol. lb, No. 1, 1996 |
