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Yonago Acta medica 2003;46:65Ð75

Slow and Fast Oscillation Electrooculography in Central Retinal Vein Occlusion: A Comparison between Affected and Fellow Intact Eyes

Machiko Inoue, Akihiko Tamai*, Shiro Hatta† and Yuji Sasaki† Clinic of , Hamada National Hospital, Hamada 697-8511, *Clinic of Ophthal- mology, Hino Hospital Association Hino Hospital, Tottori 689-4504 and †Division of Ophthal- mology and Visual Science, Department of Medicine of Sensory and Motor Organs, School of Medicine, Tottori University Faculty of Medicine, Yonago 683-8504 Japan

Using an automated electrooculograph, the Nidek EOG-2, slow and fast oscillations (SO and FO) of an electrooculogram (EOG) were recorded in 21 patients with unilateral, ischemic central retinal vein occlusion (CRVO). Patient age ranged from 49 to 81 years (average: 68 years of age). Fellow eyes in all patients were intact, and served as controls. Results showed that the L/DSO (the light peak/dark trough ratio of the SO), the RfFO [the average ratio in percentage of the maximum amplitude in the dark period (AD)/the mini- mum amplitude in the light period (AL) during FO measurement], the dfFO (the average difference in µV between AD and AL), and the df/mFO [the percentage ratio of the dfFO to the average amplitude of AD + AL (m)] were significantly decreased in the affected eyes compared with the fellow eyes. These results suggest that with regard to SO and FO origin and occurrence, the outer layer of the retina, especially the basal membrane of the retinal pigment epithelium or the choroid may be involved in the etiology of CRVO. These findings correlate with the grade of microcirculatory disturbance or ischemia in the inner layer of the retina. Furthermore, a statistically significant difference was detected in the correlation between each FO parameter and corrected visual acuity at the time of examination of the affected eyes. There was no significance between the SO parameter and the visual acuity. Therefore, it might be possible to presume that the FO parameters can be used as indicators for detecting the severity of macular functional disturbance and predicting the visual outcome for this entity.

Key words: central retinal vein occlusion; electrooculogram; fast oscillation; retinal pigment epithe- lium; slow oscillation

Central retinal vein occlusion (CRVO) results from lamina cribrosa. CRVO provides 2 forms of clinical a thrombotic occlusion, most commonly due to presentation, that is, a mild form of non-ischemic arteriosclerosis-related thrombus at the level of the CRVO (also known as partial, incomplete, hyper- Abbreviations: AD, maximum amplitude in the dark period; AL, minimum amplitude in the light period during FO measurement; BRVO, branch retinal vein occlusion; CRAO, central retinal arterial occlusion; CRVO, central retinal vein occlusion; dfFO, average difference in µV between AD and AL during the FO measurement; df/mFO, percentage ratio of the dfFO to the average amplitude of AD + AL (m); EOG, electrooculogram; ERG, electroretinogram; FO, fast oscillation; L/DSO, light peak/dark trough ratio of the SO; RfFO, average ratio in percentage of AD/AL; SO, slow oscillation 65 M. Inoue et al. permeable or venostatic retinopathy), and a severe all of whom had deteriorated EOGs in varying form of ischemic CRVO (complete or hemorrhagic degrees. Papakostopoulos and others (1992) re- CRVO) (Hayreh, 1983; Ohba, 2002). ported that the light peak/dark trough ratio of the Clinical and experimental evidence indicates SO (L/DSO) of the EOG (Arden et al., 1962) was that non-ischemic CRVO is caused by a mild oc- significantly reduced in the affected eyes of a group clusion of the central retinal vein, but that ischemic of patients with CRVO compared with the un- CRVO is caused by a severe or complete occlusion affected fellow eyes. of the central retinal vein associated with retinal The fast oscillation (FO) of the EOG, which is ischemia or significant hypoxia (Hayreh et al., the rapid initial deflection of opposite polarity oc- 1989). In a histopathologic study, Green and others curring at the initial stage of the light and dark peri- (1981) found that 13.8% of CRVO patients were ods in the EOG procedure (Kolder and Brecher, associated with central retinal arterial occlusion 1966) also showed abnormal FO patterns in patients (CRAO), and 10.8% with branch retinal artery oc- with ischemic retinopathy or CRAO (Thaler et al. clusion. Although the central retinal artery supplies 1977; Tamai et al., 1997). blood only to the inner retinal layers, simultaneous Our previous study in patients with BRVO or occlusion of the central retinal vein and artery re- CRVO (Tamai et al., 1997) suggests that analysis of sults in damage to all layers of the retina, including the SO and FO of the EOG may provide informa- the retinal pigment epithelium. tion regarding the dysfunction of the stratiform The electroretinogram (ERG) is reported to be layer in the affected retina (Hara et al., 1991) and helpful in predicting a visual prognosis in CRVO choroid. because its response is sensitive to retinal ischemia In the present study, the SO and FO variables (Henkes, 1953; Sabates et al., 1983; Sakane et al., are compared with those of the contralateral intact 1989; Ohn et al., 1991) which may be one of the eyes in patients with unilateral, ischemic CRVO, important factors for visual outcome. The ordinary with special emphasis on the corrected visual acuity slow oscillation (SO) of the electrooculogram at the time of EOG examination of the affected (EOG) on the other hand reflects the function of the eyes. retinal pigment epithelium and photoreceptor com- plex, and appears to be unrelated to the neural net- work whose function is controlled mainly by retinal Patients and Methods circulation. However, it is well established that the EOG becomes very abnormal in CRAO, the sever- Patient selection est form of retinal ischemia, and therefore the EOG appears to be indirectly related to or governed by Twenty-one patients (12 men, 9 women; age range retinal circulation (Thaler and Heilig, 1977). 49Ð81 years, mean 68 years) with unilateral, ische- Branch retinal vein occlusion (BRVO) does mic CRVO were randomly chosen for EOG record- not give proof of any abnormalities on the ERG or ing over the past 4 years (August 1996 to September EOG unless the lesion is sufficiently large, because 2000) at the Department of Ophthalmology, Tottori the ERG and EOG reflect the mass activity of the University Hospital (Table 1). Under the ophthal- retina (Karpe and Uchermann, 1955; Arden et al., moscope, it was revealed that their fundi in the af- 1962; Hara and Nagatomo, 1995). On the contrary, fected side showed a flame-shaped bleeding in the in his original description of the EOG, Arden whole retina and a remarkable papilloedema, asso- described a patient with CRVO whose EOG was ciated with dilated and tortuous retinal veins and severely deteriorated (Arden et al, 1962). Carr and lots of cotton-wool patches. Fluorescein angiog- Siegel (1964) found abnormal EOGs in CRVO raphy revealed evidence of extensive retinal capil- where the ERG remained relatively normal. lary non-perfusion in their fundi. Duration from Ashworth (1966) reported 4 patients with CRVO, onset estimated to be 5 to 167 days averaging 30.9

66 EOG slow and fast oscillations in CRVO

Table 1. Clinical data of 21 patients with unilateral, ischemic CRVO at the time of EOG examination

Patient Duration from Corrected number Age (year) Sex Affected onset (day) visual acuity General complication 174Female Right 34 0.1 Hypertension 2 68 Male Left 26 0.1 Hypertension 3 54 Female Left 11 1.2 4 71 Male Left 58 0.01 5 66 Male Left 5 0.1 Hypertension 673Female Right 8 0.7 Hypertension 7 68 Female Left 39 0.2 860Male Right 10 0.3 Hypertension 971Male Right 21 0.02 10 81 Female Left 14 CF* 11 78 Female Right 123 0.5 12 72 Male Right 13 0.02 13 49 Male Right 32 0.04 Hypertension 14 63 Male Left 12 0.4 15 70 Female Left 167 0.01 16 59 Male Right 8 0.01 Hypertension 17 71 Male Left 17 0.06 Hypertension 18 81 Female Right 6 0.04 19 74 Female Left 15 0.01 20 68 Male Right 16 0.1 21 58 Male Left 14 0.5 Hypertension *CF, counting figers: estimated to be 0.001. days at the time of EOG examination. Nine out of background luminance of 1,270 lux, when mea- the 21 patients had hypertension as a general com- sured at the location of the patient’s eyes. plication (Table 1). Fellow eyes in all patients were For every patient, cup-shaped silver-silver ophthalmoscopically and fluorescein-angiograph- chloride conductive electrodes, 8 mm in diameter, ically intact, and served as controls. were placed beside both canthi of each eye on the Patients were excluded from this study if they orbital margin, and a grounding electrode, with the had an opaque media, a bilateral refractive error same cup shape, was placed on the left earlobe, as difference of more than 3 diopters, diabetes mellitus routinely used. Before setting these electrodes, the or a history of ocular surgery, photocoagulation, skin was cleaned with 90% alcohol, and then elec- anticoagulant therapy or fibrolytic therapy. trodes were applied with a conductive paste. Elec- trode resistance was below 10 kΩ. Before SO recording, a 10-min adaptation SO and FO recordings period at a background luminance level of 1,270 lux Using a newly devised automated electrooculo- was given to the patients. Then the patients were graph, the Nidek EOG-2 (Nidek, Gamagori, Japan) instructed to fixate alternately on a pair of targets on (Nakao et al., 1995), the SO and FO were recorded the screen inside the dome. The 2 targets sub- in each patient. The EOG-2 consists of a dome, a stended 40û to the eye, and were presented alter- personal computer, an index controller, an amplifi- nately with a frequency of 0.5 Hz. er, a printer and an EOG pen recorder. Inside the On the SO recording, where 20 min of dark- dome is a hemispheric screen with a radius of 300 ness was followed by 20 min of illumination, EOG nm. Four tungsten lamps (115 V, 50 W) produce a measurements were started 40 s before the end of

67 M. Inoue et al.

AD1 AD2 AD3 AD4 AD5

AL1 AL 2 AL 3 AL 4 AL 5 Fig. 1. Fast oscillation (FO) pa- rameters, the RfFO, the dfFO and the df/mFO, calculated in this survey. AD1 AD2 ADn AD, maximum amplitude during ++ ¥ ¥ ¥ + ()AL1 AL 2 AL n the dark period; AL, minimum am- RfFO = × 100 (%) n plitude in the light period during FO measurement; n, number of (AD1 Ð AL1) + (AD2 Ð AL 2) + ¥ ¥ ¥ + (ADn Ð AL n) cycles (dark-light period of 1 min df =(µV) FO n each), 10 cycles in total.

dfFO df/mFO = × 100 (%) (AD1 + AL1 + AD2 + AL 2 + ¥ ¥ ¥ + ADn + AL n) / 2n

(10 ≥ n ≥ 3) each 1-min period during the dark and light adapta- The time constant of the amplifier was set at 3 s, and tions. Six out of 10 EOG amplitudes were automat- a high frequency cutoff of Ð3 dB was set at 20 Hz ically averaged and recorded every 1 min through for both SO and FO recordings. the EOG artifact rejection system on the Nidek Pupillary dilation provides better control of EOG-2. Twenty out of the 21 patients gave reliable retinal illumination levels, but prolongs the time for data on the test. the EOG examination and may make the examina- The SO shows a trough in the dark adaptation tion somewhat more uncomfortable for some pa- (dark trough) and a peak in the light adaptation tients. Therefore, the SO and FO recordings were (light peak) in response to dark and light periods of performed with pupils undilated. approximately 12.5 min each. The L/DSO develop- The FO parameters were calculated referring ed by Arden and others (1962) was automatically to the report by De Rouck and Kayembe (1981). calculated as an SO parameter in the present survey. Namely, the RfFO, which is the average ratio in Then the FO was recorded in all patients. percentage of the maximum amplitude in the dark Before the FO recording, the patients were subject- period (AD)/the minimum amplitude in the light ed to a 10-min pre-light adaptation in the same man- period (AL), and the dfFO, which is the average ner as in the SO recording. The 2 targets subtended difference in µV between AD and AL during the FO 40û to the eye, and were presented alternately with a measurement, were calculated in addition to a new- frequency of 0.5 Hz. The dome was periodically ly designed df/mFO, which is the percentage ratio of illuminated for 1 min followed by 1 min of dark- the dfFO to the average amplitude of AD + AL (m), ness. The measurements were started 40 s after only if at least 3 successive steps showed some each dark or light period began. There were 10 identical amplitude change (Fig. 1). Dated and measurements in each dark or light period as in the occasional large amplitude changes were not taken SO recording. The mean of the 6 EOG amplitudes into account. In the df/mFO, the influence of fluctu- recorded at the end of each dark or light period was ation of the base value to the FO pattern is supposed automatically calculated. to be minimized compared to the dfFO (Nakao et al., In this study, the calibration sensitivity for the 1995; Tamai et al., 1997). pen recorder was 200 µV/division on the printer.

68 EOG slow and fast oscillations in CRVO

(µV)SO (µV) FO 1200 R 1000 R L L 1000 800 800 600 600 400 400

EOG amplitude EOG amplitude 200 200

0 0 DDLL 0102030400 5 101520 (min) (min) Time Time

Fig. 2. EOG slow oscillation (SO) and fast oscillation (FO) patterns in both eyes of Patient 8 (60-year-old male, ischemic CRVO patient). R, right eye (affected side); L, left eye (fellow intact side). D, dark period; L, light period (horizontal axis).

All values were expressed as mean ± SD. Results Statistical analysis was performed with Mann- Whitney’s U test. Spearman’s rank coefficient of Practical EOG SO and FO patterns in both eyes of correlation test was applied for correlation analysis. Patient 8 (a 60-year-old male patient with uni- A P value of < 0.05 was considered statistically lateral, ischemic CRVO) are demonstrated in Fig. 2. significant. In this patient, reduced or deteriorated SO and FO patterns were observed in his affected eye (right eye), although his fellow intact eye (left eye) show- ed normal patterns in both

± recordings. 3.0 Affected eye Fellow intact eye Mean SD (n = 20) 1.38 ± 0.37 1.93 ± 0.33 * L/D 2.5 *P < 0.01 SO Figure 3 shows the dis- 2.0 tribution of the L/DSO in 20 affected and fellow in- SO 1.5 tact eyes of 20 patients with ischemic CRVO ex- L/D cluding 1 patient (Patient 1.0 10), whose data were un- reliable. Nineteen out of 0.5

0 1234567 8910111213141516 17 18 19 20 21 (patient number) Patients

Fig. 3. Distribution of the L/DSO of the EOG in 20 affected and fellow intact eyes of 20 patients with ischemic CRVO. The ratios in Patient 10 were omitted due to unreliable data.

69 M. Inoue et al.

(%) Affected eye Fellow intact eye ± 145 Mean SD (n = 21) 117.3 ± 10.3 140 125.9 ± 11.2 * *P < 0.05 135

130

125 FO 120 Rf

115

110

105

100 1234567 891011121314151617 18 19 20 21 (patient number) Patients

Fig. 4. Distribution of the RfFO of the EOG in 21 affected and fellow intact eyes of 21 patients with ischemic CRVO. the 20 patients (95.0%) showed smaller ratios in the RfFO L/DSO in the affected eyes than those in the fellow healthy eyes. The mean of the L/DFO of all affected Figure 4 shows the distribution of the RfFO in 21 eyes was 1.38 ± 0.37 (SD), and of all fellow intact affected and fellow intact eyes of the 21 patients eyes was 1.93 ± 0.33. This difference is statistically with ischemic CRVO. Eighteen out of the 21 significant (P < 0.01). patients (85.7%) showed smaller values in the RfFO

µ ( V) ± 300 Affected eye Fellow intact eye Mean SD (n = 21) 85.6 ± 52.7 168.9 ± 60.5 * 250 *P < 0.01

200

150 FO df

100

50

0 1234567 891011121314151617 18 19 20 21 (patient number) Patients

Fig. 5. Distribution of the dfF0 of the EOG in 21 affected and fellow intact eyes of 21 patients with ischemic CRVO.

70 EOG slow and fast oscillations in CRVO

Affected eye Fellow intact eye Mean ± SD (n = 21) 15.0 ± 8.8 (%) * 40 22.3 ± 8.0 *P < 0.01 35

30

FO 25

20 df/m

15

10

5

0 1234567 891011121314151617 18 19 20 21 (patient number) Patients

Fig. 6. Distribution of the df/mFO of the EOG in 21 affected and fellow intact eyes of 21 patients with ischemic CRVO.

in the affected eyes than those in the fellow healthy eyes. The mean of the df/mFO of all affected eyes eyes. The mean of the RfFO of all affected eyes was was 15.0 ± 8.8%, and of all fellow intact eyes was 117.3 ± 10.3%, and of all fellow intact eyes was 22.3 ± 8.0%. This difference was statistically 125.9 ± 11.2%. This difference was statistically significant (P < 0.01). significant (P < 0.05).

dfFO

Figure 5 shows the distribution of the dfFO in 21 2.5 affected and fellow intact eyes of the 21 patients y = 1.66 + 0.25 log (x) with ischemic CRVO. Twenty out of the 21 pa- r = 0.46 Correlation analysis (P > 0.05) tients (95.2 %) showed smaller values in the dfFO in the affected eyes than those in the fellow healthy 2

eyes. The mean of the dfFO of all affected eyes was SO 85.6 ± 52.7 µV, and of all fellow intact eyes was L/D 168.9 ± 60.5 µV. This difference was statistically 1.5 significant (P < 0.01).

1 df/mFO CF 0.01 0.1 1.0

Figure 6 shows the distribution of the df/mFO in 21 Corrected visual acuity at the examination affected and fellow intact eyes of the 21 patients Fig. 7. Correlation between the L/DSO and corrected vi- with ischemic CRVO. Eighteen out of the 21 pa- sual acuity at the time of EOG examination in 20 affect- tients (85.7%) showed smaller values in the df/mFO ed eyes of 20 patients with ischemic CRVO. CF, count- in the affected eyes than those in the fellow healthy ing fingers (estimated to be 0.001).

71 M. Inoue et al.

(%) (µV) 150 y = 125.6 + 7.06 log (x) 250 r = 0.53 140 Correlation analysis (P < 0.05) 200 y = 126.3 + 34.6 log (x) 130 r = 0.51 150 Correlation analysis (P < 0.05) FO

120 FO df Rf 100 110

50 100

90 0 CF 0.01 0.1 1.0 CF 0.01 0.1 1.0

Corrected visual acuity at the examination Corrected visual acuity at the examination

Fig. 8. Correlation between the RfFO and corrected vi- Fig. 9. Correlation between the dfFO and corrected vi- sual acuity at the time of EOG examination in 21 affect- sual acuity at the time of EOG examination in 21 affect- ed eyes of 21 patients with ischemic CRVO. CF, count- ed eyes of 21 patients with ischemic CRVO. CF, count- ing fingers (estimated to be 0.001). ing fingers (estimated to be 0.001).

On the other hand, a statistically significant Correlations between the SO parameter and difference was detected in the correlation between corrected visual acuity and between each FO each parameter (Rf , df and df/m ) and correct- parameter and corrected vision FO FO FO ed visual acuity at the time of EOG examination in No significant difference was detected in the corre- the 21 affected eyes of the 21 patients with ischemic lation between the SO parameter (L/DSO) and cor- CRVO (P < 0.05) (Figs. 8 to 10). rected visual acuity at the time of EOG examination in the 20 affected eyes of the 20 patients with ische- mic CRVO (P > 0.05) (Fig. 7). Discussion

(%) Arden and others (1962) postulated that the SO is 40 y = 22.55 + 6.39 log (x) related to slower changes in potential that occur as a r = 0.57 Correlation analysis (P < 0.05) result of alterations in the metabolism of the retinal 30 pigment epithelium. They suggested that normal magnitudes of corneoretinal potential are depen-

FO dent on i) normally functioning photoreceptors, ii) 20 normally functioning retinal pigment epithelium,

df/m iii) normal contact between the sensory neuroepi- 10 thelium and the retinal pigment epithelium and iv) adequate choroidal blood supply.

0 Concerning the origin and occurrence of the CF 0.01 0.1 1.0 FO, Steinberg and others (1983) reported the in- Corrected visual acuity at the examination volvement of the retinal pigment epithelium, main- ly in its basal membrane. Joseph and Miller (1991) Fig. 10. Correlation between the df/mFO and corrected visual acuity at the time of EOG examination in 21 af- suggested that the FO might result from delayed hy- fected eyes of 21 patients with ischemic CRVO. CF, perpolarization associated with increased electric counting fingers (estimated to be 0.001). resistance in the basal membrane of the retinal pig-

72 EOG slow and fast oscillations in CRVO ment epithelium. This delayed basal membrane hy- same functional insufficiency of the whole retina perpolarization may be caused by a decrease in in- due to an overflow of glutamic acid (Honda, 1996). tracellular chloride of the retinal pigment epi- Furthermore, the participation of nitric oxide thelium, which is linked to the light-induced drop in (NO) may disturb the condition of the retinal pig- subretinal potassium concentration (Joseph and ment epithelium and Müller’s cell (Honda, 1996). Miller, 1991). An increase in concentration of intracellular cal- In the present study, results showed that the L/ cium ([Ca2+]i) may also bring about cellular damage DSO, the RfFO, the dfFO and the df/mFO were signifi- in occlusive retinal vascular diseases (Honda, cantly decreased in the affected eyes of the patients 1996). Other reasons, including morphological as compared with the fellow intact eyes. These re- changes resembling apoptosis-like cell death, have sults suggest that with regard to SO and FO origin been considered, but the real causes which bring and occurrence, the outer layer of the retina, espe- about such EOG changes in these diseases have not cially the basal membrane of the retinal pigment yet been elucidated. In any case, the EOG changes epithelium or the choroid may be involved in the may be helpful for better understanding of the etiology of CRVO. These findings correlate with pathogenesis of CRVO. the grade of microcirculatory disturbance or ische- It is of note that a statistically significant dif- mia in the inner layer of the retina. ference was detected in the correlation between As for the influence of retinal bleeding, a de- each FO parameter and corrected visual acuity at crease in illuminating volume may bring an indirect the time of EOG examination of the affected eyes of or direct influence on the EOG responses, especial- the patients. There was no significance between the ly in patients with hemorrhagic or ischemic CRVO. SO parameter and the visual acuity. Rods as well as Its influence seems to be very small and negligible cones contribute to the FO (Welber, 1989), while in these patients because their retinal bleeding re- cones as well as rods contribute to the SO (Arden mains flame-shaped in their fundi. and Kelsey, 1962; Gouras and Carr, 1965). There- The EOG responses may be affected by changes fore, such a cone-dominated activity on the FO in in the retrobulbar circulation due to a systemic hy- this series is currently unexplainable, but it might pertensive condition more or less associated with be possible to presume that the FO parameters can occlusive retinal vascular diseases and/or arterial be used as indicators for detecting the severity of blood flow characteristics, that is, reduction of macular functional disturbance and predicting the blood flow velocities in the central retinal and oph- visual outcome for this entity. thalmic arteries especially in patients with ischemic Generally, visual prognosis is obviously poor- CRVO, which may be partly related to secondary er in ischemic CRVO than in non-ischemic CRVO changes in the retrobulbar circulation as a result of due to severe retinal bleeding and edema especially enhanced arterial resistance following CRVO in the macular area. Ischemic CRVO sometimes (Anunduk et al., 1999). leads to the recovery of visual acuity in parallel With regard to influences from anemia or with absorption of retinal bleeding and disappear- ischemia, elevation of the osmotic pressure in the ance of cystoid macular edema after panretinal subretinal space may bring an unstable retinal pig- photocoagulation. Ischemic CRVO often leads to ment epithelium. Decrease of the oxygen quotient visual disturbance due to vitreous bleeding caused may bring a functional insufficiency in the outer by neovascularization from the retina and optic disk retinal layers (Honda, 1996). An increase in the as well as macular edema (Kanski, 1989), and may volume of ammonia in the ischemic retina may lead to rubeosis iridis and to potentially painful neo- bring a functional insufficiency of the whole retina vascular glaucoma resulting in visual loss in older due to an overflow of glutamic acid. Oxidized persons (Deng et al., 1994; Papakostropoulos et al., stress after ischemic reperfusion may also bring the 1992).

73 M. Inoue et al.

Further work is required to investigate these stract). aspects and the variation of the EOG with time, for 12 Hayreh SS. Classification of central retinal vein oc- the results above represent readings taken at only clusion. Ophthalmology 1983;90:458Ð474. 13 Hayreh SS, Klugman MR, Podhajsky P, Kolder HE. one point in the natural history of the condition. in central retinal vein occlusion. Correlation of electroretinographic changes with pupillary abnormalities. Graefes Arch Clin Exp Acknowledgments: The authors thank Professor Ophthalmol 1989;227:549Ð561. Yoshitsugu Inoue, Division of Ophthalmology and Vi- 14 Henkes HE. Electroretinography in circulatory dis- sual Science, Department of Medicine of Sensory and turbances of the retina. I. Electroretinogram in cases Motor Organs, School of Medicine, Tottori University of occlusion of the central retinal vein or one of its Faculty of Medicine, for his generous help. branches. Arch Ophthalmol 1953;49:190Ð201. 15 Honda Y. Cellular and molecular biology of ische- mic retina. Nippon Ganka Gakkai Zasshi 1996;100: References 937Ð955 (in Japanese with English abstract). 16 Joseph DP, Miller SS. Apical and basal membrane 1 Arden GB, Barrada A, Kelsey JH. New clinical test ion transport mechanisms in bovine retinal pigment of retinal function based upon the standing potential epithelium. J Physiol 1991;435:439Ð463. of the eye. Br J Ophthalmol 1962;46:449Ð467. 17 Kanski JJ. Retinal vein occlusion. Clinical ophthal- 2Arden GB, Kelsey JH. Some observations on the mology. 2nd ed. London: Butterworths; 1989. p. relationship between the standing potential of the 318Ð328. and the bleaching and regeneration of 18 Karpe G, Uchermann A. The clinical electroreti- visual purple. J Physiol 1962;161:201Ð226. nogram. Acta Ophthalmol 1955;33:156Ð493. 3Ashworth B. The electro-oculogram in disorders of 19 Kolder HE, Brecher GA. Fast oscillations of the

the retinal circulation. Am J Ophthalmol 1966;61: corneoretinal potential in man. Arch Ophthalmol

ˆ 505Ð508. ˆ 1966;75:232Ð237. 4 Avunduk AM, Dinç H, Kapicioglu Z, Ugurlu S, 20 Nakao H, Miki N, Nagata M, Sasaki Y, Yamasaki A, Dayanir V, Korkmaz E. Arterial blood flow charac- Endo M, et al. Fast oscillations of the electro-oculo- teristics in central retinal vein occlusion and effects gram in a series of normal subjects. Jpn J Ophthal- of panretinal photocoagulation treatment: an inves- mol 1995;39:113Ð119. tigation by color Doppler imaging. Br J Ophthalmol 21 Ohba N. Central retinal vein occlusion. Essential 1999;83:50Ð53. atlas of retinal diseases. Kagoshima: Shibundo; 5 Carr RE, Siegel IM. Electrophysiologic aspects of 2002. p. 35Ð36. several retinal diseases. Am J Ophthalmol 1964;58: 22 Ohn Y-H, Katsumi O, Kruger-Leite E, Larson EW, 95Ð107. Hirose T. Electrooculogram in central retinal vein 6 Deng Y, Zhou H, Duan J. Electro-oculogram of occlusion. Ophthalmologica 1991;203:189Ð195. retinal vein occlusion. Eye Science 1994;10:60Ð64. 23 Papakostopoulos D, Bloom PA, Gray RHB, Dean 7 De Rouck, Kayembe D. A clinical procedure for the Hart JC. The electro-oculogram in central retinal simultaneous recording of fast and slow EOG vein occlusion. Br J Ophthalmol 1992;76;515Ð519. oscillations. Int Ophthalmol 1981;3:179Ð189. 24 Sabates R, Hirose T, McMeel JW. Electroretino- 8 Gouras P, Carr RE. Cone activity in the light- graphy in the prognosis and classification of central induced DC response of monkey retina. Invest Oph- retinal vein occlusion. Arch Ophthalmol 1983;101: thalmol Vis Sci 1965;4:318Ð321. 232Ð235. 9 Green WR, Chan CC, Hutchins GM, Terry JM. 25 Sakane H, Katsumi O, Hirose T. Electroretino- Central retinal vein occlusion: a prospective histo- graphic findings in fellow eyes of patients with cen- pathologic study of 29 eyes in 28 patients. Trans Am tral retinal vein occlusion. Arch Ophthalmol 1989; Ophthalmol Soc 1981;79:371Ð422. 107:1459Ð1462. 10 Hara A, Nagatomo M. Branch retinal vein occlusion 26 Steinberg Rh, Linsenmeier RA, Griff ER. Three light- decreases the potential of the inner retinal layer. J evoked responses of the retinal pigment epithelium. Nippon Med Sch 1995;62:50Ð54 (in English). Vision Res 1983;23:1315Ð1323. 11 Hara A, Nohmi M, Sato M. Electrooculogram in 27 Tamai A, Sasaki Y, Inoue M, Hamamoto J, retinal branch vein occlusion. Ganka Rinsho Iho Kumagami T, Setogawa A, et al. Clinical applica- 1991;85:123Ð126 (in Japanese with English ab- tion of fast oscillation of electro-oculogram. Ganka

74 EOG slow and fast oscillations in CRVO

Rinsho Iho 1997;91:535Ð538 (in Japanese with Eng- 30 Welber RG. Fast and slow oscillations of the electro- lish abstract). oculogram in Best’s macular dystrophy and retinitis 28 Thaler A, Heilig P. EOG and ERG components in pigmentosa. Arch Ophthalmol 1989;107: 530Ð537. ischemic retinopathy. Ophthalmic Res 1977;9:38Ð 46. 29 Thaler A, Heilig P, Scheiver V. Fast oscillation of Received May 28, 2003; accepted July 16, 2003 the corneoretinal potential in ischemic retinopathy. Ophthalmic Res 1977;9:324Ð328. Corresponding author: Akihiko Tamai, MD

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