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1 From the Retina Foundation of the Southwest, Dallas, Texas; and the 2 Department of Ophthalmology, University of Texas Southwestern Medical Center, Dallas.
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Abstract |
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METHODS. Subjects were patients with RP who had acuity 
20/32 and no visual
field defects within 6° from the fovea. Maxwellian-view and
direct-view optical systems were used to obtain foveal and extrafoveal
TCSFs under a range of test conditions, including high retinal
illuminances that yielded temporal contrast sensitivity independent of
mean retinal illuminance. TCSFs were described using log sensitivity
and corner frequency parameters.
RESULTS. Foveal TCSFs in these patients showed overall reductions in sensitivity but no frequency-dependent defects. Also, no macular defects were found in the timing of the multifocal ERG. TCSFs from extrafoveal locations in moderate field defects, obtained at retinal illuminances that were sufficient to render flicker sensitivity independent of effective mean luminance, showed reductions in overall sensitivity as well as changes in temporal tuning. The multifocal ERGs from these extrafoveal locations showed signs of temporal slowing.
CONCLUSIONS. Changes in temporal tuning (both psychophysical and electroretinographic) were found only within visual field scotomas, whereas changes of the log sensitivity parameter were found also in the relatively preserved foveas of this group of patients with early stage RP.
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Introduction |
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Abnormalities in photopic flicker sensitivity in RP have also been found using psychophysical techniques. Several behavioral studies have addressed changes in temporal processing in patients with RP, reporting reduced temporal contrast sensitivity,10 delayed impulse response functions,11 but normal temporal integration12 in patients with RP.
It would be useful to establish a link between retinal function and visual function, which would help the understanding of the ERG and the development of sensitive psychophysical tests. However, the relationship between abnormalities in the flicker ERG and altered psychophysical temporal processing is complicated. First, several different factors can cause the alterations in ERG and psychophysical thresholds that are typical in RP. Elevated psychophysical thresholds may be due to a reduced number of photoreceptors or to a reduction in quantum catch of the photoreceptors (e.g., due to misalignment of the cones,13 or to shortened cone outer segments14 ). A delay in the implicit time of the flicker ERG may be the result of slowing of the transduction process, or of a loss of sensitivity of the transduction process.15 Furthermore, recent reports indicate that at least part of the flicker ERG signal originates from postsynaptic processes,16 rather than from the cone photoreceptors. Psychophysical thresholds presumably represent a combination of retinal and cortical filtering. Additionally, both psychophysical thresholds and the time course of the ERG are known to vary across the retina (or, correspondingly, the visual field) in normals, and even more so in patients with RP.
Second, large interindividual variability in the relationship between psychophysical sensitivity and ERG measures has been reported among patients with RP,17 even in data from patients with the same mode of inheritance of RP (autosomal dominant, autosomal recessive, or X-linked recessive), or from patients with the same known mutation.17 18 19
The first aim of this study was to investigate early changes in foveal temporal contrast sensitivity due to RP, using stimulus conditions and patient selection criteria that were designed to help distinguish between the possible causes of the psychophysical abnormalities mentioned above. From a large patient population we selected patients with early stages of RP who had good acuity and many of whom showed no signs of reduced quantum catch of the foveal cones.20 Our second aim was to reduce the effects of retinal inhomogeneities on the comparison between psychophysical measures and the ERG. Using optimized stimulus conditions, extrafoveal temporal contrast sensitivity functions (TCSFs) were obtained from specific regions of the retina that were selected on the basis of the patients’ multifocal ERGs and visual fields.
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Methods |
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This study followed the tenets of the Declaration of Helsinki. Informed written consent was obtained from all subjects after the nature and possible consequences of the study were explained. This research was approved by the Institutional Review Board of the University of Texas Southwestern Medical Center at Dallas.
Apparatus
A two-channel Maxwellian-view optical system with a 2–mm
artificial pupil was used to obtain foveal TCSFs in experiment 1. The
test was provided by a diffused light-emitting diode (LED) in the first
channel, controlled by a Macintosh II computer with an AO-6 12-bit,
6-channel analog output (National Instruments, Austin, TX) and a
high-speed DMA-8 timing board (National Instruments). The LED was
linearized using a pulse-density method described
elsewhere.21
A diffused tungsten light source in the
second channel provided the surround. The lights from the two channels
were combined by a photometric cube and passed through a 570–nm
interference filter, resulting in a 2°–diameter uniform circular
test field yielding a mean retinal illuminance of 50 Td (1.7 log Td),
surrounded by a 10° square, steady field of 35 Td. The fairly dim
green test was chosen to avoid effects of long-wavelength
adaptation.22
23
For experiments 2 and 3, which involve parafoveal and extrafoveal stimuli, a direct-view optical system was used. A diffused green LED, controlled as described above, subtended 4° of visual angle and had a maximum mean luminance of 160 cd/m2, thus yielding a uniform maximum mean retinal illuminance of 3.9 log Td for an 8-mm-diameter pupil (taking into account the Stiles–Crawford effect24 ). The surround was formed by a large white screen with a luminance of 170 cd/m2. Subjects fixated the LED for the foveal measurements. For extrafoveal measurements a fixation mark was placed on the white screen, such that the stimulus would fall in the visual field location of interest.
Psychophysical Procedures
In all psychophysical experiments a temporal 2-alternative
forced-choice (2AFC) paradigm was used. A computer-generated voice
indicated the beginning of each stimulus interval and provided feedback
after each trial. In each measurement 2 staircases for different
frequencies were run in a randomly interleaved manner with 10 reversals
each, after a 2-down/1-up rule. Contrast changed in octave steps,
changing to half-octave steps after the second reversal. For
measurements of the critical flicker frequency (CFF), the test
frequency was varied initially in steps of 2 Hz, and in steps of 1 Hz
after the second reversal. Threshold was defined as the 75%-correct
point of a 3-parameter Weibull function that was fit to the data using
maximum likelihood estimation.25
All testing was done
monocularly. For the direct-view stimuli (experiments 2 and 3),
subjects were dilated and subjectively refracted in the apparatus.
Stimulus Conditions
Obtaining reliable psychophysical threshold data from a patient
population requires careful stimulus design. The forced-choice paradigm
was adopted to minimize the variability resulting from inter- and
intraindividual differences in decision criteria.
The 2AFC paradigm entails choosing a finite temporal waveform of the
stimuli instead of continuous stimulation. At high test frequencies a
small bandwidth is desired to prevent biased results at the steep
fall-off of the De Lange curve. However, small bandwidth stimuli
involve larger numbers of cycles, which may become problematic at low
frequencies, for which this results in long durations. Patients may not
be able to fixate properly for the duration of each stimulus
presentation. Also, the total duration of the experiment may become a
limiting factor, because relatively large numbers of presentations are
needed for reliable data in a clinical population. Furthermore,
long-duration stimuli may cause adaptation effects.26
27
Here, a trade-off was made between the temporal frequency bandwidth and
the duration of the stimuli. Two types of temporal waveform were used.
In experiment 1, which included relatively low test frequencies, the
waveform was the 6th derivative of a gaussian (D6 pattern), which is a
relatively "short" waveform and has a fixed bandwidth of 1
octave.28
For the subsequent measurements, in which only
CFF (experiment 2) or only the high-frequency portion of the TCSF
(experiment 3) was obtained, the waveform was a temporal Gabor pattern,
defined as
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was set at 20, resulting in a fixed
bandwidth of 0.24 octaves. To avoid effects of mean retinal illuminance (e.g., due to changes in optical density of the cones) in the extrafoveal measurements of experiment 3, relatively bright stimulus conditions were chosen. For increasing mean retinal illuminance, temporal contrast sensitivity for a given test frequency first increases and then levels off to a constant level,29 30 31 32 and thus becomes independent of mean retinal illuminance. Furthermore, this asymptote is reached at higher values of mean retinal illuminance for increasing temporal (and spatial) frequency of the stimulus.32 Therefore, when mean luminance becomes high enough that CFF levels off to an asymptote, contrast sensitivity for all lower frequencies should also be independent of mean luminance. Accordingly, for most subjects this asymptotic behavior was verified for CFF only. For a small number of normal subjects asymptotic behavior was verified for the entire TCSF once CFF had reached an asymptotic value (results not shown).
Data Analysis
All TCSFs were fit with a linear-filter model. The individual data
from experiment 1, which included relatively low test frequencies, were
fit by a three-parameter model defined as the difference of two
n-stage linear filters, for which the amplitude response
equals:
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The CFF-vs-retinal illuminance functions (experiment 2) were fit with a
Michaelis–Menten function
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Experiment 1: Foveal TCSFs
To study abnormalities in foveal temporal contrast sensitivity in
patients with relatively preserved macular function, foveal TCSFs were
obtained in 9 patients with RP (age, mean ± SD, 38.3 ± 6.8
years) and 10 age-similar normals (age, 39.4 ± 8.6 years). 2AFC
contrast thresholds for 2° diameter D6 stimuli were measured for test
frequencies ranging from 1.4 to 22 Hz and CFF. The Maxwellian-view
optical system was used for this experiment. Mean luminance of the test
field was 50 Td.
All 9 patients in experiment 1 had participated in an earlier study,20 which found Rayleigh matches within the normal range, indicating that the most sensitive foveal cones of these patients did not have reduced optical densities.
Experiment 2: CFF as a Function of Retinal Illuminance
To study the asymptotic behavior of temporal contrast sensitivity
for increasing retinal illuminances for our stimulus conditions, CFFs
were measured in 15 patients (age, 40.9 ± 10.7 years) and 16
age-similar normals (age, 41.9 ± 10.5 years) for a range of mean
luminances, starting at 1.5 log units (or occasionally 2.0 or 2.5 log
units) below maximum, and increasing in 0.5 log steps to the maximum
mean luminance of 160 cd/m2. Using the
direct-view optical system, CFFs were obtained for Gabor stimuli at
each luminance level, for foveal and 5° extrafoveal test locations on
the horizontal meridian of the temporal retina.
Experiment 3: TCSFs in Relative Scotomas
A subgroup of the patients in experiment 2, consisting of 6
subjects (age, 41.0 ± 7.2 years; selected on availability and
willingness to undergo further testing), participated in experiment 3.
Results were compared with the results from 6 age-similar normals (age,
41.5 ± 7.1 years).
The multifocal ERG technique37 was used to obtain responses from 103 locations across the central retina. In short, the stimulus was presented at 200 cd/m2 mean luminance on an M2400 black and white monitor (Dotronix, New Brighton, MN), and consisted of a 47° by 39° two-dimensional hexagonal array of 103 elements. The luminance of each element was alternated between 400 and 0.4 cd/m2 in a pseudorandom sequence (m-sequence) at the frame refresh rate of the monitor (75 frames per second). Stimulus control and data collection were performed by VERIS Scientific software (Electro-Diagnostic Imaging, San Mateo, CA). A Burian–Allen contact lens electrode was used to record the corneal ERG from one eye with dilated pupil, refracted for the test distance.
On the basis of the multifocal ERG results and the results of automated
static perimetry (24-2 threshold program on an HFA 640 perimeter;
Humphrey Systems, Dublin, CA) one location in the visual field of each
patient was selected for further psychophysical testing. This location
showed a delay 5 msec in the peak of the multifocal ERG but no
absolute defect in the visual field (<1.0 log unit threshold elevation
for 3 patients, and 1.0–1.5 log unit elevation for 2 patients), and
was typically around 10° eccentricity. Control data were obtained in
locations of corresponding eccentricity in the normal subjects. To
improve signal-to-noise, multifocal ERG responses were averaged over 7
hexagons centered on the extrafoveal test location. For comparison, the
macular (i.e., central) 7 hexagons of each multifocal ERG were also
averaged.
Using the direct-view optical system, the high-frequency portion of the TCSF was measured using 4° diameter temporal Gabor stimuli at the maximum mean luminance of 160 cd/m2 for frequencies ranging from 14 to 40 Hz in half-octave steps. Note that only the high-frequency portion of the TCSF was measured. To verify that the mean luminance was sufficient to bring CFF in or near the asymptotic region, CFFs were obtained at the maximum mean luminance (160 cd/m2), and at 1.0 and 0.5 log units below the maximum.
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Results |
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97%. The foveal TCSFs obtained in experiment 1 are shown in Figure 1 for normals (Fig. 1A) and patients (Fig. 1B) . Interindividual variability in the patient group appears to be larger than in the normals; TCSFs tend to be lower in the patients than in the normals; but at CFF no obvious differences between the groups are readily seen in Figure 1 . Fits of the linear filter model to the data are also given in Figure 1 . The three-parameter model produced reasonable fits for each data set, capturing individual differences in shape and sensitivity of the TCSFs (Fig. 1) .
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Discussion |
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In an attempt to minimize this interindividual variability in our study population, strict selection criteria were applied. In particular, patients with field defects entering the macula were excluded, to avoid large variability in patients’ macular visual function. Note here that this exclusion criterion was based on a different visual field measure than parameters typically used, which describe the "amount" of field loss in patients with RP. Massof et al.40 calculated the total area of the remaining visual field, including any peripheral islands. Sandberg et al.17 used a similar parameter and converted this into an "equivalent field diameter." Both of these methods ignore the shape of the visual field or the distribution of scotomas. Conversely, the "nearest field defect" criterion adopted here contains no information about the total area or the extent of the remaining visual field. (For comparison, an estimate of the more widely used equivalent field diameter for each patient is given in Table 1 . The correlation between the equivalent field diameter and the flicker ERG amplitude was borderline significant; P = 0.054.)
The patients that participated in experiment 1 were examined previously20 to estimate cone optical density. None showed signs of reduced optical density. Of the 9 patients tested in experiment 1, 3 showed reduced sensitivity, but 0 showed altered temporal tuning of the foveal TCSF. Dagnelie and Massof11 measured foveal TCSFs in a group of patients with RP of various pathophysiological and inheritance subtypes. They found reductions of flicker sensitivity that after transformation to the time domain showed delays in the impulse response function, corresponding to a reduction in corner frequency. Earlier, Tyler et al.10 found reductions of foveal temporal contrast sensitivity in RP that were more pronounced for frequencies above 10 Hz than for lower frequencies. This, also, indicates a shift of the TCSF along the frequency-axis rather than the sensitivity-axis. Both these studies may have included patients with field defects close to the macula. Tyler et al.10 included patients with Goldmann visual field radii of 2° and larger. In the study by Dagnelie and Massof11 disease severity was reported in terms of years past critical age, which is based on total area of the remaining visual field40 and hence contains no information on the distribution of defects across the visual field.
A crucial parameter that varied across these studies, as well as the experiments reported here, is the mean retinal illuminance at which the results were obtained. Tyler et al.’s10 experiments were performed at a maximum mean luminance of 40 cd/m2, which for the reported pupil diameters of 8 to 9 mm corresponds to a retinal illuminance of approximately 3 log Td (taking into account the Stiles–Crawford effect24 ). Dagnelie and Massof11 measured at 500 Td (2.7 log Td). TCSFs shift to lower temporal frequencies when retinal illuminance is reduced.41 More importantly, the "effective" mean retinal illuminance may vary within each of these studies if the patients tested have reduced quantum catch of the cones. Thus, alterations in temporal tuning of the TCSF could have been caused by reductions in cone optical density. Patients with RP who have retained good acuity may have a 0.3 log unit reduction in foveal cone optical density.42 43 (To simulate the effects of the resulting change in effective mean retinal illuminance, we obtained foveal TCSFs in 9 young normal observers at mean retinal illuminances of 50 Td and 25 Td. The results confirmed a significant effect of mean retinal illuminance on corner frequency in our test conditions; t = 3.50, P = 0.008.)
We also studied functional characteristics of selected extrafoveal retinal locations corresponding to moderate field defects (threshold <1.5 log units above mean normal). Because cone optical density is likely to be reduced in these locations, relatively bright stimulus conditions and dilated pupils were used, which rendered the TCSFs independent of effective retinal illuminance. Graham and Hood32 give an extensive review of normal data that show a transition from "constant amplitude threshold" behavior to "constant contrast threshold" behavior with increasing luminance. This transition implies that temporal contrast sensitivity reaches an asymptotic value at high retinal illuminances. Such asymptote has also been found in X-linked dichromats35 and in patients with RP.7 35 We found this asymptotic behavior for normals and for patients with RP (experiment 2), assuring that the maximum mean luminance of our direct-view stimuli was sufficiently high to bring subjects in or near this asymptotic region.
The transition to "constant contrast threshold" behavior is known to occur for higher illuminances at higher temporal frequencies. Therefore, if the mean retinal illuminance is not quite sufficient to reach asymptotic CFF for a given patient for a given retinal location, constant contrast threshold behavior may hold at lower temporal frequencies, whereas constant amplitude threshold behavior holds at higher temporal frequencies. A reduction of cone optical density would then affect contrast sensitivity at higher frequencies more than at lower frequencies, resulting in a reduced corner frequency of the TCSF.
Of the six patients for which TCSFs were obtained from extrafoveal locations corresponding to field defects (experiment 3), three patients showed altered temporal tuning (corner frequency below 95% confidence limit for normal) of the TCSF measured from a defective area of the visual field, and two patients scored at the lower end of the normal range. Note here that patient 3206 showed a reduced corner frequency (Fig. 7 , right) but normal sensitivity (Fig. 6B) . However, CFF was not quite in the asymptotic range for this patient at the retinal location tested (Fig. 5) , and the abnormal corner frequency could therefore be due, in part, to a reduction in cone optical density.
Summarizing our psychophysical results, we found significant changes in temporal contrast sensitivity in this group of patients with RP. Abnormalities in TCSFs obtained from areas that were normal on perimetry (i.e., these patients’ foveas) appeared to be reductions in log sensitivity rather than corner frequency, whereas the abnormalities in TCSFs corresponding to extrafoveal field defects showed a combination of changes in log sensitivity and corner frequency. We must restate here, however, that a clear understanding of the results is hampered by interindividual variability, even though the spread of the log sensitivity and corner frequency values in the patient group is not much larger than in the normal group. Figure 8 shows the TCSF parameters obtained here as a function of the clinical visual function data presented in Table 1 . A hint of a relationship is seen between the foveal corner frequency parameter and the distance to the nearest visual field defect, between the extrafoveal corner frequency and the visual field diameter, and between the extrafoveal log sensitivity and the two flicker ERG parameters. However, no significant correlation was found between any of the TCSF and clinical visual function parameters. Although this may be attributed in part to the relatively small number of patients in this study, the much larger study by Dagnelie and Massof11 also found rather poor correlation between similar TCSF attributes and visual field area. (Their test conditions and inclusion criteria were somewhat different from ours, however, and only foveal data were reported; See comments above.) The poor correlation is therefore more likely to be due to interindividual variability,17 18 19 reflecting the notion that the physiological processes that underlie each of the parameters tested do not necessarily have similar spatial distributions across the retina and/or follow the same time course in patients with RP.
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When the present ERG findings are compared with our psychophysical results, we see reduced sensitivity but normal timing of the foveal TCSFs in combination with normal timing of the multifocal ERG, and extrafoveal TCSFs with reduced sensitivity and abnormal timing combined with delays in the timing of the multifocal ERG. We conclude therefore that abnormalities in the flicker ERG implicit time are related to changes in temporal tuning of the psychophysical TCSF, provided that retinal illuminance is sufficiently high to yield constant contrast threshold behavior. Alterations in the timing of the multifocal ERG in patients with RP have been shown to be multiplicative45 46 rather than additive, indicating a slowing of the response rather than a simple delay. This may be due, in part, to a broadening of the impulse response of the cones, which, in turn, would cause the psychophysical corner frequency to be reduced. However, a quantitative relation was not found between the timing of the peak of the multifocal ERG and either psychophysical corner frequency or log sensitivity parameters.46
A model for changes in the TCSF that includes both sensitivity and corner frequency parameters follows from the assumption that achromatic temporal contrast is processed via the magnocellular pathway, which is mediated by the parasol retinal ganglion cells. The receptive field centers of these ganglion cells receive input from several cone photoreceptors. If only a small fraction of the cones in a given region of the retina are damaged (i.e., not functioning or functioning abnormally), the flickering stimulus may be mediated by parasol ganglion cells whose receptive field centers have lost input from a few, but not all, cones. Because the input to such ganglion cell is proportional to the number of cones feeding into its receptive field, a greater stimulus increment is needed for the subject to perceive flicker. This would correspond to a decreased sensitivity in this region of the retina. However, assuming that detection of the stimulus in this case is mediated by remaining "healthy" cones, the temporal response properties will still be determined by these remaining cones and therefore not necessarily abnormal. Thus, it is feasible that sensitivity changes occur while temporal tuning is unaltered in early stages of photoreceptor damage. When a larger fraction of cones in a given region of the retina function abnormally, which is possibly the case for mild visual field defects, the flicker stimulus may be mediated by parasol ganglion cells whose receptive field receives input from mostly abnormal photoreceptors. Beside a further decrease in sensitivity, temporal response properties may in this case be determined by predominantly "sick" photoreceptors. Note here that this latter case would still be considered a relatively early stage of photoreceptor damage.
In summary, the cause of reductions in psychophysical flicker sensitivity in RP may depend on the mean retinal illuminance. Abnormalities may be related to reduced cone optical density for values of retinal illuminance in the constant–amplitude range, and related to temporal dysfunction of the cones in the constant–contrast range. Furthermore, the TCSF, visual field, and ERG parameters discussed here correlate poorly, supporting the idea that the underlying physiological processes do not change hand-in-hand during the progression of RP.
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Acknowledgements |
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Footnotes |
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Submitted for publication April 13, 1998; revised November 19, 1998 and May 18, 1999; accepted July 21, 1999.
Commercial relationships policy: N.
Corresponding author: Joost Felius, University of Michigan, W. K. Kellogg Eye Center, 1000 Wall Street, Ann Arbor, MI 48105. E-mail: jfelius{at}umich.edu
3 Present address: SUNY College of Optometry, 100 E. 24th Street, New York, NY 10010. 
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0.21.
3.2
log Td. Each panel contains the data for one subject. Solid
lines correspond to best fits of the linear filter model
described in the text. Goodness-of-fit: Individual residual standard
deviations all 
