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1 From the Department of Psychology, Columbia University, New York, New York; the 2 Department of Ophthalmology, New York University Medical Center, New York, New York; the 3 Department of Ophthalmology, College of Physicians and Surgeons, New York, New York; and the 4 New York Eye and Ear Infirmary, New York, New York.
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Abstract |
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 Top Abstract IntroductionMethodsResultsDiscussionAuthors’ NotesReferences |
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METHODS. Multifocal VEPs were recorded from both eyes of six normal subjects and four patients; each eye was stimulated separately. Two of the patients had glaucoma, one had ischemic optic neuropathy, and one had unilateral optic neuritis. All four patients had considerably more damage in one eye than in the other, as indicated by their Humphrey visual fields. The multi-input procedure of Sutter was used to obtain 60 VEP responses to a scaled checkerboard pattern. The amplitude in each response was obtained using a root mean square measure of response magnitude. For each of the 60 pairs of responses, a ratio between the amplitude of the responses from the two eyes was obtained as a measure of the relative health of one eye compared with the other. The mean and SD of this ratio measure for the control group were used to specify confidence intervals for each of the 60 locations. All patients had Humphrey 24-2 visual fields performed. To allow a comparison of the mVEPs to the visual fields, a procedure was developed for displaying the results of both tests on a common set of coordinates.
RESULTS. Except for a small interocular difference in timing attributable to nasotemporal retinal differences, the pairs of mVEP responses from the two eyes of the control subjects were essentially identical. Many of the pairs of responses from the patients were significantly different. In general, there was reasonably good agreement with the Humphrey 24-2 visual field data. Although some regions with visual field defects were not detected in the mVEP due to small responses from the better eye, other abnormalities were detected that were hard to discern in the visual fields.
CONCLUSIONS. Local monocular damage to the ganglion cell/optic nerve can be quantitatively measured by an interocular comparison of the mVEP.
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionAuthors’ NotesReferences |
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A potential way around intersubject variability is to compare, within a subject, the two sets of mVEP records obtained by stimulating each eye separately. Although the mVEP responses differ among individuals, the mVEP responses from both eyes of the same individual should be very similar if both eyes are healthy. The anatomic basis for this statement is well known. Although points in the visual field fall on different hemi-retinas of the two eyes, they project to the same cortical location. For example, a point in the left visual field falls on the temporal retina of the right eye and on the nasal retina of the left. But these corresponding retinal points project via ganglion and geniculate cells to cortical regions within a few hundred microns of each other. Thus, in principle, if the optics, retina, and pathways are functioning equally well in both eyes, then the mVEP should be the same from both eyes when referenced to the stimulus location in the visual field. In practice, this would fail to be true if the nasal and temporal retinal inputs to the cortex were different or if one eye dominated the VEP because of an asymmetry in the input. However, if the monocular mVEP responses from the two eyes of control subjects are reasonably similar, then a comparison of the two monocular mVEP recordings from patients may allow the detection of early and localized damage of the ganglion cells or optic pathway. Early signs of these diseases are unlikely to be identical in the temporal retina of one eye and the nasal retina of the other.
One purpose of this study is to determine the degree to which the mVEP responses from the two eyes of normal subjects agree. We find that interocular differences do exist. However, these differences are subtle and will not interfere with the ability of this technique to detect optic nerve damage. A second purpose is to develop methods to quantify interocular differences in the mVEP obtained from patients. Finally, the third purpose is to present the interocular mVEP differences in a form that will allow for easy comparison to local sensitivity changes as measured with the Humphrey visual field analyzer. These methods are illustrated with four patients with diseases of the ganglion cells/optic nerve.
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Methods |
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The stimulus array was displayed on a black and white monitor driven at a frame rate of 75 Hz. The monitor had a resolution of 1024 x 768 pixels, and the check inside the smallest sector had an average of approximately 20 pixels. The 16-element checkerboard of each sector had a probability of 0.5 of reversing on any pf frame change, and the pattern of reversals for each sector followed a pseudorandom (m-) sequence. For a more detailed description of the general multifocal technique see Refs. 8 9 and 14 ; for more on the mVEP see Refs. 7 10, and 15.
Electrode Placement
An electrode was placed 4 cm above the inion and referenced to an
electrode placed at the inion. A forehead electrode served as the
ground. All responses in the figures are displayed with the reference
(inion) electrode as negative. Following the suggestion of Klistorner
et al.,10
we also tried lowering the electrode pair such
that the reference fell 2 cm below the inion and the active 2 cm above.
A comparison of these two electrode placements was made by
simultaneously recording the mVEP from both configurations. In five of
the seven control subjects run in this experiment, the records were
essentially identical. One of the other two subjects showed larger
responses to one placement, whereas the other showed larger responses
to the other. For this group of seven individuals, there was no
advantage to placing an electrode below the inion. Furthermore, this
placement has the disadvantage of being more difficult to apply and
maintain.
Recordings
To obtain an mVEP, the continuous VEP record was amplified with
the low- and high-frequency cutoffs set at 3 and 100 Hz (1/2 amplitude;
Grass preamplifier P511J; Quincy, MA), and it was sampled at 1200 Hz
(every 0.83 msec). The m-sequence had 216
-1 elements and required approximately 14.5 minutes for a single run.
The records presented in the figures are the average of two of these
runs. To improve the subject’s ability to maintain fixation, the run
was broken up into overlapping segments each lasting approximately 27
seconds. Second-order local response components were extracted using
VERIS 3.0 software from EDI. All other analyses were done with programs
written in MATLAB (Mathworks, Natick, MA).
Displaying the Responses
Figure 1B
contains the records from one of the control subjects.
For clarity of presentation, the positions of the individual records do
not correspond to the locations of the sectors in Figure 1A . To allow
the reader to make comparisons between the mVEP from the two eyes and
to increase the signal-to-noise ratio, the mVEP responses were grouped
and averaged. The 16 groups are shown in Figure 1D
, which, unlike
Figure 1A
, is not drawn to scale. Twelve of these groups had four
responses (see group 15 in Figs. 1B
and 1D
), whereas the middle four
groups had three responses. The responses from the upper field are
usually reversed in polarity from those in the lower
field.7
10
15
16
In our experience the responses along the
vertical midline can also differ in waveform from other responses. The
groups, in general, respect these differences. The exception can be
found for the central four groups; in some subjects they may be
averages of responses that differ in waveform. Because we felt it
important to allow the reader to see the comparisons between the
records from the two eyes, this exception for some subjects seemed a
small price to pay at this stage of the development of the technique
(the typical VEP, of course, is a single response averaged across the
entire area tested). In any case, a summary measure of all 60 responses
is shown in Figure 5
.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionAuthors’ NotesReferences |
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There are various ways to measure these responses. A common measure of response magnitude, called amplitude here, is the root mean square (RMS) calculated over some time interval (see note 1). The RMS has the advantage that it does not depend on the identification of a particular aspect of the response waveform but merely requires the specification of a time interval. The choice of the interval is not particularly critical for the purposes of this study. We used the interval from 45 msec, where the mVEP is first obvious, to 120 msec, a time after the major positive peak occurs in control subjects. The relative size of the responses from the two eyes was obtained as the ratio of the RMS value from the right to that from the left eye. On average, responses from the two eyes were about the same amplitude; the mean for all 60 RMS ratios was 1.05 (SD = 0.16). The log of the OD/OS RMS ratio was used as the measure of relative response at each field location for both the controls and patients. This log scale has the advantage of being symmetrical around a mean of 0. That is, if the responses from the two eyes are of the same amplitude, then the log ratio is 0; and if one eye has twice the amplitude of the other, then the log ratio is either 0.3 or -0.3 depending on which eye has the larger response. The log scale has the further advantage of being comparable to the log scale (in decibels) of the Humphrey field.
Nasotemporal Retinal Differences
There is a small but consistent difference between eyes that can
be seen in all subjects. Notice in Figures 2C
and 2D
that the responses
along the midline from the left eye (red) tend to lead the responses
from the right (blue) eye in the left visual field and follow them in
the right visual field. This timing difference was quantified by
shifting the grouped responses on a time axis to bring them into
register with each other. This required a mean shift of 4.8 msec
(SD = 1.0 msec) for the six control subjects. These differences in
timing do impose a practical limitation. They preclude a comparison of
the two eyes via subtraction of the mVEP responses. Subtracting the
responses of one normal eye from the other produces surprisingly large
differences for the more peripheral midline locations due to these
small latency differences. The basis of these differences in latency
will be considered in the Discussion section.
Detecting Abnormal mVEP Responses
The grouped mVEP responses from the four patients are shown in
Figures 2E
2F
2G
2H
. All 60 pairs of responses for patient P3 are
shown in Figure 3B
. These patients were chosen because their visual
fields indicated that the damage to one eye was considerably greater
than to the other eye. Figure 4
shows the total deviation plots from the Humphrey 24-2 fields for both
eyes of the patients. Virtually all points in the field of the more
affected eye showed a greater loss in sensitivity than the other eye.
As will be seen below there is a minor, but interesting, exception in
the case of P4.
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Probability Plots for the mVEP
The right-most column of Figure 5
presents the mVEP results for all 60 pairs of responses for each of the
patients. Each square locates the center of one of the 60 sectors of
the stimulus display. The black squares indicate that the response
ratio was within 2 SD of the control values. The colored squares
indicate that the response ratio was more than 2 SD (lighter
desaturated color) or 3 SD (darker saturated color) from the mean of
the controls. The color denotes whether the right (blue) or left (red)
eye had the larger response. The results are similar to those for the
grouped data. The ratios more than 2 SD from the controls are nearly
always associated with the more affected eye as identified by the 24-2
fields. As will be seen below, the red squares in the mVEP of P4 in
Figure 5H
are not false positives. In the case of P3, the two red
squares may be false positives, although the central one replicated
when this patient was tested 6 months later.
A Qualitative Comparison between mVEP and Visual Fields
Although the mVEP probability plots in Figure 5
can be compared
with the Humphrey probability plots in Figure 4
, the Humphrey field
data also can be represented as interocular difference fields so as to
make the comparison to the mVEP easier. The left-most column of Figure 5
shows probability plots for the difference between the Humphrey
visual fields from the two eyes. Figure 6 illustrates how these were obtained. Figures 6A
and 6B
show the
deviation values for P1’s left and right eyes. These values underlie
the plots in Figure 4
. They are part of the standard printout of the
Humphrey visual field report and represent the difference in decibels
between the patient’s threshold values at each test location and the
age-corrected normal values for that location. Figure 6C
is simply the
difference between these numbers. These numbers represent how much
worse relative to normal is the left eye, compared with the right eye.
To obtain the interocular probability plots for the Humphrey 24-2
visual fields in Figure 5
(left-most column), the points were coded
assuming that the SD is 2.8 dB. The SD will not be the same at every
location, but 2.8 dB is a reasonable estimate (see note 2). For the
three patients with largely unilateral damage (P1, P2, P3), these plots
should resemble the deviation plots in Figure 4
for the more affected
eye. In fact, fewer points show up as significantly different largely
because the better eye in the patient had points slightly (i.e., 1–3
dB) less sensitive than the control values (e.g., see Fig. 6B
).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionAuthors’ NotesReferences |
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One purpose of the present study was to determine the extent to which mVEP responses obtained from two eyes of subjects with normal vision agree. The results showed that the pairs of responses tend to be very similar; the interocular comparisons were far more similar than any intersubject comparisons. It is important in interpreting these results to keep in mind that any given pair of responses reflects cortical activity from essentially the same cortical region, but that the two responses originate from different parts of the retinas of the two eyes. Recall that any point in the visual field falls on the temporal retina of one eye but on the nasal retina of the other. Yet, despite coming from different retinal locations and traveling via different pathways (crossed versus uncrossed), the mVEP responses are essentially identical in control subjects. We did find small differences in latency across the midline of these responses. These latency differences were in the range of approximately 5 msec and probably reflect a small difference in the time it takes signals to arrive at V1 from the nasal as opposed to the temporal retina. Most likely, this small difference is due to the conduction time of the unmyelinated ganglion cell axons on the retinal surface. The action potentials from the ganglion cells in the temporal retina travel farther to the optic disc than do the action potentials from corresponding points on the nasal retina (see review in Ref. 18) . Whatever the source of these differences, they are small and do not affect the usefulness of the interocular comparison.
Our second purpose was to explore a method for quantifying the differences between the two eyes. The RMS ratio measure appears to work well. Here the RMS value in an interval from 45 to 120 msec was taken as our response measure. This interval allows for detection of delays in the responses as well. For example, in Figure 2F , the responses in the upper left field for P2 are outside 2 SD because the response from the affected eye is delayed, causing it to fall partially beyond the 45 to 120 msec window. It is likely that, in at least some cases, a different time interval or different measure may better discriminate between affected and less affected or nonaffected regions of the two eyes. However, it is clear that the mVEP responses from the two eyes can be quantitatively compared. Furthermore, this quantitative measure correctly identifies the more affected eye, as defined by the Humphrey visual field results.
Comparison of mVEP Fields to Visual Fields
Our third purpose was to present the mVEP in a form that allows
comparisons to visual fields. The probability plots in Figure 5
allow a
comparison to the probability plots of Figure 4
. An interocular 24-2
probability plot was devised to make the plots more directly
comparable. In general, the agreement between the mVEP and visual field
plots is good. However, there are places where the visual field shows a
difference between the two eyes, but the mVEP does not, and other
places where the reverse is the case. To understand these
discrepancies, it is necessary to keep in mind the problems and
assumptions involved in comparing mVEP and visual field measures. Below
we consider four reasons why such discrepancies might exist.
First, each measure has its own sources of variability, and the test giving the more reliable results may depend on the subject. In the case of visual field measures, results for some subjects may have a low reliability due to excessive fixation losses, false-negative error rates, and/or false-positive error rates. On the other hand, it may be more difficult to detect differences in the mVEP in some subjects than in others due to muscle artifacts, alpha waves, and cortical anatomy.
Second, local discrepancies between mVEP and visual fields may exist because the data from some field locations may be less reliable than data from other locations. The peripheral locations of the Humphrey visual field are occasionally unreliable due to occlusion by anatomic facial features or due to the difficulty some patients have in judging the presence or absence of peripheral lights. Some locations give less reliable mVEP responses because of the orientation of their primary visual area in the cortex. These areas include the upper field, central fovea, and midline. Notice in Figure 5 that P1, P3, and P4 all have locations in the upper field that are significantly different in the visual field plot but not the mVEP plot. This is in part attributable to the smaller and more variable mVEP responses from the upper field (see Fig. 3A ).
A third possible explanation for the discrepancies between mVEP and visual field probability plots is that the mVEP may detect pathologic changes where none are apparent in the visual field. The Humphrey visual fields can be within the normal range even when the ganglion cells show substantial damage.19 The mVEP from the patient with optic neuritis illustrates this point well.
Finally, the discrepancies may be due to the underlying assumptions made to compare visual fields to mVEP responses. We assume that the threshold measured with the 24' Humphrey test spot is a good proxy for the sensitivity of the immediate region. If half the ganglion cells are missing in that region, then it should follow that the mVEP will be smaller, perhaps by one half. However, it is less clear how this will affect visual field sensitivity. In the extreme, if the damage is uneven with islands of either good or bad sensitivity, then, depending on where the 24' test spot falls, the visual field sensitivity could be either better or worse than indicated by the mVEP. The results from P4 illustrate this point. Here the mVEP suggests that her more affected eye (OS) has a region of good vision (the red region in Fig. 5H ) that is not apparent in her 24-2 field of Figure 4D . Figure 7 shows a Humphrey visual field for her left eye obtained with 103 test locations.20 The field has an island of near normal sensitivity (white area) surrounded by a large region of depressed sensitivity (black region). The agreement with the mVEP probability plot is quite good.
In summary, the interocular analysis of the mVEP suggested here allows for an objective and quantitative identification of monocular field defects. Because the analysis depends on a comparison of the mVEP responses from corresponding points in the visual field, it cannot detect abnormalities that would affect these points equally. In particular, damage to corresponding points in the nasal retina (or optic nerve) of one eye and the temporal retina (or optic nerve) of the other, as well as damage to the optic tract beyond the optic chiasm, would go undetected. However, this leaves a wide range of possible clinical and basic science applications. For clinical purposes, the recording sessions used here are probably too long. The records in this study were obtained with 30 minutes of recording. But for clinical testing and screening, it should be possible to substantially reduce the recording time. Whether the mVEP technique will prove more useful in some cases than other traditional tests such as the visual field remains to be determined. The results here are encouraging enough to warrant using this technique on patients who show little or no visual field loss.
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Authors’ Notes |
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TopAbstractIntroductionMethodsResultsDiscussionAuthors’ NotesReferences |
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The ratio of the RMS values of the right eye to the left
eye was calculated as
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Acknowledgements |
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Footnotes |
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Submitted for publication June 30, 1999; revised September 27, 1999; accepted November 16, 1999.
Commercial relationships policy: N.
Corresponding author: Donald C. Hood, Department of Psychology, 406 Schermerhorn Hall, 116th Broadway, Columbia University, New York, NY 10027. don{at}psych.columbia.edu
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TopAbstractIntroductionMethodsResultsDiscussionAuthors’ NotesReferences |
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A. I. Klistorner and S. L. Graham Electroencephalogram-Based Scaling of Multifocal Visual Evoked Potentials: Effect on Intersubject Amplitude Variability Invest. Ophthalmol. Vis. Sci., August 1, 2001; 42(9): 2145 - 2152. [Abstract] [Full Text] [PDF]
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D. C. Hood, J. G. Odel, and X. Zhang Tracking the Recovery of Local Optic Nerve Function after Optic Neuritis: A Multifocal VEP Study Invest. Ophthalmol. Vis. Sci., November 1, 2000; 41(12): 4032 - 4038. [Abstract] [Full Text]
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D. C. Hood, V. C. Greenstein, K. Holopigian, R. Bauer, B. Firoz, J. M. Liebmann, J. G. Odel, and R. Ritch An Attempt to Detect Glaucomatous Damage to the Inner Retina with the Multifocal ERG Invest. Ophthalmol. Vis. Sci., May 1, 2000; 41(6): 1570 - 1579. [Abstract] [Full Text]
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