Download Simultaneous pattern reversal ERG and VER recordings

Investigative Ophthalmology & Visual Science, Vol. 31, No. 3, March 1990
Copyright © Association for Research in Vision and Ophthalmology
Simultaneous Pattern Reversal
ERG and VER Recordings
Effect of Stimulus Field and Central Scotoma
Hiroshi Sakaue, Osamu Karsumi,* Mehul Mehra, and Torsuo Hirose*t
The effects of the sizes of the stimulus field and of an artificially created central scotoma on simultaneously recorded pattern-reversal electroretinogram (P-ERG) and pattern-reversal visual-evoked response (P-VER) were investigated. With an increase in the stimulus field from 4° X 4° to 12° X 12°,
the amplitude of the P-ERG increased steadily. The amplitude of the P-VER also showed an increase
up to a stimulus field of 6° X 6° or 8° X 8°, but showed no increase with further expansion of the
stimulus field. A central scotoma, created by placing a square of black paper at the center of the 12°
X 12° stimulus field, was increased from 4° X 4 ° t o l O ° X 10° by 2-degree increments. Amplitudes of
both the P-ERG and the P-VER decreased with increasing central scotoma size. The P-VER decreased significantly with a 4° X 4° central scotoma. Although both the P-ERG and the P-VER were
influenced by the overall stimulus field and the central scotoma, there was a distinct difference in their
behavior. The P-VER showed saturation above a certain stimulus field size and, with a central scotoma
of 4° X 4°, much more reduction than the P-ERG, suggesting that the P-VER depends more on the
macular area than does the P-ERG. The P-ERG also exhibited a substantial macular dependency,
which, however, was not as great as that of the P-VER. The greater macular dependency of the P-VER
compared to the P-ERG, as observed in our study, reflects the larger anatomic representation of the
macula at the higher visual level. Invest Ophthalmol Vis Sci 31:506-511,1990
The pattern-reversal electroretinogram (P-ERG),
originally introduced by Riggs et al,1 was made popular by the work of Maffei and Fiorentini,2 who concluded that the P-ERG originates in the retinal ganglion cells. The origin of the P-ERG is controversial,
however; Dodt3 postulated that the P-ERG may be
generated in proximal retinal layers and consists of
both a local luminance component at high stimulus
contrasts and a pattern component at low stimulus
contrasts. The nature of the P-ERG remains obscure.
P-ERG is not applied in routine clinical settings, although its use in the early detection of glaucoma4"6
and in optic nerve disease7"9 has been studied.
Since the original work of Spekreijse,10 numerous
studies have been performed on the effects of various
stimulus parameters on the recordability of the pattern-reversal visual-evoked response (P-VER). The
P-VER is used widely now in ophthalmology clinics,
especially to evaluate the visual pathway and macular
function."12
The P-VER is influenced significantly by various
stimulus parameters, including the overall stimulus
field and the presence of a central scotoma.1314 Relatively few investigations have studied the effect of
stimulus field and central scotoma on the P-ERG,15
and even fewer have studied the differences between
the modes of response in simultaneously recorded
P-ERGs and P-VERs.16"18
We believed that before the P-ERG, which is more
difficult to record, is applied clinically, the different
responses of the P-ERG and the P-VER to these parameter changes should be studied more precisely.
Therefore, we compared the responses of the P-ERG
and the P-VER to changes in the stimulus field size
and the central scotoma size, using different methods
from previous work.16"18
From the Eye Research Institute of Retina Foundation and *Retina Associates, and the fDepartment of Ophthalmology, Harvard
Medical School, Boston, Massachusetts.
Submitted for publication: November 21, 1988; accepted June
12, 1989.
Reprint requests: Osamu Katsumi, MD, Eye Research Institute
of Retina Foundation, 20 Staniford Street, Boston, Massachusetts
02114.
Materials and Methods
Four normal adults (three men and one woman
ranging in age from 24 to 33 yr) participated. They
had no ophthalmologic abnormalities except for a
slight refractive error that was corrected optically at
the time of the recordings. Prior to the examination,
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SIMULTANEOUS PATTERN REVERSAL ERG AND VER RECORDINGS / 5ohoue er ol
the procedure was explained fully to all subjects, and
their informed consent was obtained.
P-ERG and P-VER were recorded simultaneously
with two-channel recordings. The left eye always was
tested with a natural pupil. For the P-ERG, a soft
piano contact lens electrode (Model Breath-O; Toray,
Tokyo, Japan) developed by Yanashima and Okisaka19 was placed in the subject's left eye after instillation of 1% proparacaine hydrochloride. The image
of the checkerboard pattern viewed through this contact lens was sharp. The reference electrode for the
P-ERG was placed on the center of the left lower lid,
and the earlobes served as grounds. For the P-VER,
Ag-AgCl disc type electrodes (Grass Instrument,
Quincy, MA) were used. The active electrode was
placed at Oz (10% of the inion-nasion distance from
the inion on the midline), and the reference electrode
was placed at Pz (30% of the inion-nasion distance
from the inion on the midline). The ground electrodes were the same as those of the P-ERG.
A 9-inch television monitor (model 2640 C9;
Conrac, Covina, CA) was used for stimulus display.
The overall stimulus field size was 12 cm X 12 cm
with a cardboard border to eliminate contamination
from distorted peripheral checks. The stimulus field
size subtended a visual angle of 12° x 12° from a
viewing distance of 57 cm. The mean luminosity
level was 50 cd/m2 (1.2 log fL), and the contrast was
maintained at 90%. The stimulus pattern was
a square-wave checkerboard with a check size of
60 min of arc.
The checkerboard pattern alternating speed was 2
Hz (4 reversals per sec), and analysis time was 200
ms. Responses were fed into the averaging computer
(Cadwell model Quantum 84; Cadwell Laboratories,
Kennewick, WA) after amplification through highcut and low-cut filter settings of 70 Hz and 1 Hz,
respectively. The 256 responses were averaged and
printed out with a plotter.
Figure 1 illustrates the various stimulus modes
used in this investigation. To study the effect of the
overall stimulus field size, we increased the field from
4 ° X 4 ° t o l 2 ° X 1 2 o b y 2-degree increments, using
frames of thick black paper. A small black fixation
target was placed at the center of each stimulus field.
Then a central scotoma was created by placing thick
black paper of various sizes at the center of a 12°
X 12° stimulus field. The size was increased from 4°
X 4° to 10° X 10° by 2-degree increments. To ensure
stable fixation, a small white target was placed at the
center of each piece of black paper. The P-ERG and
the P-VER were recorded simultaneously in a dark
room.
The resulting percentage amplitudes for both field
and scotoma area were analyzed with three-factor
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50?
mixed effects analyses of variance (4 subjects X 4
areas X 2 patterns; random subjects) at a preestablished 0.05 significance level.
Results
Both the P-ERG and the P-VER with a stimulus
field of 12° X 12° showed major deflection (Fig. 2).
In the P-ERG, an initial negative deflection (Nl) appeared at about 30 ms, and a positive deflection (PI)
followed at about 50 ms. The amplitude was measured from Nl to PI. In the P-VER, an initial negative deflection (N70) appeared at about 70 ms, and a
positive deflection (PI00) appeared at about 100 ms.
The response size was calculated and served as the
P-VER amplitude (N70 - PI00).
Effect of Stimulus Field Size
Figure 3 shows the P-ERG and the P-VER amplitudes with five different stimulus field sizes tested in
four subjects. In all subjects, the amplitude of P-ERG
continuously increased, up to the largest stimulus
field size. The amplitude of P-VER also increased,
but only up to a certain stimulus field size; saturation
Stimulus Field-Size
Central Scotoma Size
12x 12
( D t g r w Squared)
4x4
(Degrees Squired)
10x10
6x6
8x8
8x8
6x6
10x10
4x4
Fig. 1. Schema of* the various modes of stimulation.
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INVESTIGATIVE OPHTHALMOLOGY 6 VISUAL SCIENCE / March 1990
P-ERG
1.25 uV
Vol. 31
toma; the reduction of P-VER amplitude was much
larger than that of the P-ERG amplitude in the four
subjects.
The relationship between the area of the central
scotoma and the P-ERG and the P-VER amplitudes
is shown in Figure 6. This difference showed a trend
toward statistical significance (F = 4.11, P < 0.053).
P-VER
20 msec
N70
J
|2.5nV
20 msec
Fig. 2. Tracings of simultaneous recordings of the P-ERG and
the P-VER with a 12° X 12° stimulus field.
1.5"
C
P-VER
1
"4 -o
1.0-
Ainpli
was observed at a field size of 6° X 6° in one subject
and at 8° X 8° in the remaining three.
Figure 4 shows the relationship between the
P-ERG and the P-VER amplitudes relative to the
area of the stimulus field in four subjects. The amplitude of the P-ERG, expressed as percent of electroretinogram (ERG) at the largest field size, steadily increased; in the P-VER, in contrast, saturation clearly
was observed beyond a stimulus field size of 8° X 8°.
In the P-ERG, the percent amplitude showed a
marked increase with the expansion of stimulus field
size. The mean percent amplitudes of both the
P-ERG and the P-VER were larger than the actual
percentage area of the stimulus field at all stimulus
field sizes. For example, with an 11% stimulus field
area (equivalent to a 4° X 4° stimulus field), the
P-VER showed 63% amplitude, whereas the P-ERG
showed 29%. The percent amplitudes of the P-VER
were significantly higher than those of the P-ERG
at all of the stimulus field sizes tested (F = 86.49,
P< 0.001).
3 g.
O 0.5-
P-ERG
OS
W
a.
o.o-
Effect of Central Scotoma Size
Figure 5 shows the P-ERG and the P-VER amplitudes with four different central scotoma sizes in four
subjects. The amplitudes of both the P-ERG and the
P-VER decreased in all subjects as central scotoma
size increased. In the P-ERG, the amplitude decreased markedly when the scotoma was larger than
6° X 6°; in the P-VER, the amplitude significantly
decreased with the 4° X 4° central scotoma, but
dropped less precipitously with larger central scotomas. The most striking difference between the
P-ERG and the P-VER occurred with a 4° X 4° sco-
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2
4
6
8
10
12
Stimulus Field Size (Degrees Squared)
Fig. 3. (A) The effect of the stimulusfieldsize tested in subject 1.
The abscissa shows the stimulus field size in degrees squared, and
the ordinates indicate the amplitudes of the P-ERG (left) and the
P-VER (right). (B, C, D) The effect of the stimulusfieldsize tested
in subjects 2, 3, and 4, respectively.
SIMULTANEOUS PATTERN REVERSAL ERG AND VER RECORDINGS / Sokoue er ol
No. 3
509
minimal interference from scattered light. At small
field sizes, our squared stimulus field could stimulate
only the macular area. Thus, our results indicate
slight macular dependency only with a small stimulus
field area; with a large stimulus field area, the relationship between the P-ERG amplitude and stimulus
field area became more linear, suggesting equal effec-
0
10 20 30 40 50 60 70 80 90 100
% Stimulus Field Area
Fig. 4. The relationship between the area of the stimulus field
and the amplitudes of the P-ERG and P-VER in four subjects. The
abscissa shows the percentage area of stimulusfield,with 12° X 12°
expressed as 100%. The ordinate indicates the amplitudes of the
P-ERG and the P-VER. The points on the lines show the mean
percent amplitudes of the P-ERG (large squares) and the P-VER
(large circles) obtained from four subjects (P-ERG, small squares;
P-VER, small circles) with five different stimulusfieldsizes.
With a central scotoma of 4° X 4° (11% decrease in
the full-field stimulus size), the reduction of mean
percent amplitude of the P-ERG was only 13%,
whereas that of the P-VER was 41%. With a central
scotoma of 6° X 6° (area decrease of 25%), the
P-ERG and the P-VER decreases were 41% and 48%,
respectively. As central scotoma size increased to 8°
X 8° (area decrease, 44%), decreases in the P-ERG
and the P-VER were 64% and 62%, respectively; at
10° X 10° (area decrease, 69%) decreases in the
P-ERG and the P-VER were 77% and 72%, respectively. The percent reductions of the mean percent
amplitudes of both the P-ERG and the P-VER were
consistently larger than those of percent area decrease
at all of the central scotoma sizes, but especially at
the central scotoma sizes equal to or smaller than
6° X6°.
Discussion
Regarding the effect of the overall stimulus field
size, we found that with smaller stimulus field sizes
the percent amplitude of P-ERG generated was larger
than the percentage of stimulus field area (29% amplitude from 11% stimulus field area and 48% amplitude from 25% stimulusfieldarea). At stimulus fields
larger than 8° X 8°, the relation became more linear
and proportional to the percentage of stimulus field
area. These results agree with thefindingsof Armington16 and Hess and Baker15 that P-ERG is fitted by a
straight line, indicating linear area summation and
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2
4
6
g
10
Central Scotoma Size (Degrees Squared)
Fig. 5. (A) The effect of the central scotoma size tested in subject
1. The abscissa shows the central scotoma size in degrees squared
and the ordinates indicate the amplitudes of the P-ERG (left) and
the P-VER (right). (B, C, D) The effects of the central scotoma size
tested in subjects 2, 3, and 4, respectively.
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / March 1990
0
10 20 30 40 50 60 70 80 90 100
(90 80 70 60 50 40 30 20 10 )
% Central Scotoma Area
(Remaining % Stimulus Field Area)
Fig. 6. The relationship between amplitudes of P-ERG and
P-VER and the area of the central scotoma. The abscissa shows the
area of central scotoma as a percentage of the full-field stimulus.
The number in parentheses indicates the remaining area (percent)
of the stimulus field. The ordinate indicates the amplitudes of the
P-ERG and the P-VER, with the full-field stimulus (12° X 12°
stimulus field) in each subject expressed as 100%. Individual subjects: P-ERG, small squares; P-VER, small circles. Means: P-ERG,
large squares; P-VER, large circles.
tiveness. In contrast, the P-VER amplitudes (63%
from an 11% stimulus field area and 77% from 25%
stimulus field area) indicate that the P-VER depends
to a greater extent on the macular area.
The most striking difference between the P-ERG
and the P-VER was saturation in the P-VER. In the
P-ERG, there was a weak tendency toward macular
dependency, but saturation was not observed in any
of the subjects. Katsumi et al14 reported that monocular P-VER with a small check size did not increase
beyond a 5° X 5° stimulus field. This saturation can
be explained by the total number of elements in the
stimulus field and the check size; when the number
exceeds a certain level, saturation occurs.20 Perhaps
our finding of P-VER saturation with a 6° X 6° or an
8° X 8° stimulus field was due to the relatively large
check size (60 min of arc) necessary for reliable PERGs.
P-VER was influenced markedly by a 4° X 4° central scotoma, as reported by Katsumi et al,14 whereas
P-ERG was less influenced by this size scotoma. With
a central scotoma of 4° X 4°, the percentage reduction of the P-ERG amplitude was 13%, while that of
the P-VER amplitude was almost 41%. Gronenberg
and Teping13 reported that the amplitude of the
P-VER from a 4° X 4° stimulus area was larger than
that from the peripheral retina outside of it. Our
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Vol. 31
study also showed that the P-VER decreased by
nearly half, in the presence of the smallest central
scotoma. The decreases in the percent amplitude of
the P-ERG (41%) and the P-VER (48%) were not
significantly different with larger central scotomas,
eg, 6° X 6°. Thus, the P-ERG was not as sensitive to a
4° X 4° central scotoma as was the P-VER, suggesting that P-VER has the greater macular dependency
of the two recordings. This agrees with Sokol's report
that P-VER is a more useful electrodiagnostic index
of macular disease than is P-ERG.17 However, our
finding that the P-ERG also showed a larger decrease
in mean percent amplitude than in percent area may
indicate that the P-ERG also has a substantial macular dependency, though not as great as that of the
P-VER. This conclusion substantiates the study of
Armington and Brigell, who concluded that macular
dependency occurred, with a ring stimulus field, because of receptor density and associated anatomic
factors of the macula.18 We agree with their explanation. The greater macular dependency of the P-VER
compared with that of the P-ERG, as observed in our
study, reflects the larger anatomic representation of
the macula at the higher visual level.
Key words: pattern reversal ERG, pattern reversal VER,
stimulusfield,central scotoma, macular function
Acknowledgments
The authors wish to thank Charles L. Schepens, MD, for
his support during this study; Armando Garsd, PhD, for his
statistical analysis; and Elizabeth W. Larson and Charlene
J. Skladzien for their technical assistance.
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