Suppression is a fundamental aspect of the visual deficit that characterizes strabismic and anisometropic amblyopia. As such, understanding and measuring suppression is key to the management of these conditions and to the restoration of binocular function. The results of a number of recent animal1–3 and human studies4–6 have highlighted the importance of suppression by supporting the idea that strabismic amblyopes have a structurally intact binocular visual system that is rendered functionally monocular as a result of the suppressive influences from the fellow fixing eye.
In the clinic, there is at present no good way of quantifying suppression as the majority of tests are largely binary in nature (i.e., suppression is either present or absent). There is a need to be able to accurately measure suppression so that different treatment regimes for the restoration of binocular vision can be evaluated. Recently, we described a novel method for the measurement of suppression,6 and we went on to show that continual and intensive measurement in itself leads to the diminution of suppression and the restoration of normal binocular function, including stereopsis.7,8 The equipment needed to accomplish this, although being ideal for the laboratory, was less than ideal for the clinic. Dichoptic stimuli (i.e., different stimuli to each eye) were presented by way of an 8-mirror haploscope (an optical instrument that allows different images to be presented to the eyes) that was large (1 × 1 × 2 m) and required ancillary equipment including a desktop computer and three computer monitors. This is clearly not compatible with a crowded consulting room. In addition, the laboratory testing routine we used was thorough but time consuming.6 There is no way that such space consuming equipment and time consuming measurements could be successful in the clinic where space and time are at a premium. Here, we describe a successful translation of this equipment and procedure into a head-mounted display (HMD) system that can be worn by the patient and run by a laptop computer. In addition, we have optimized the psychophysical procedure used to objectively assess the strength of interocular suppression and validated this optimized procedure against the more time consuming procedure we previously used. We believe this makes it possible to use our apparatus to measure suppression in the clinic and to provide ideal conditions to reduce suppression over time using our antisuppression treatment.7,8
Here, we present details of the new stimulus display apparatus along with a set of measurements made using the apparatus on five normal participants and nine amblyopic observers. Measurements were made using two psychophysical techniques. The first technique uses multiple interleaved staircases and provides a rich dataset. However, this technique is time consuming to implement. The second, new technique speeds up the procedure by implementing a staircase procedure that directly targets the suppression and, therefore, allows measurements to be made over a number of short trials. This results in a practical clinical test that could potentially be used with younger amblyopic patients.
The Head-Mounted Display
We chose to use the Z800 dual pro (eMagin, Bellevue, WA) headmounted display (HMD; Fig. 1) because its screens were composed of organic light emitting diodes (OLEDs) whose luminance response is high and linear (see calibration below) and whose response is fast enough to avoid any motion smear. The resolution is 800 × 600 pixels in each eye with a simultaneous refresh rate of 60 Hz in each eye. The dual pro version allows dichoptic presentation of visual information, which is fundamental to our approach of displaying signal motion elements to one eye and noise motion elements to the other. It can be fitted over existing spectacles, and the center-to-center distance between the left and right eye screens can be adjusted to match the interpupillary distance of each subject. We aligned stimuli in each eye under binocular viewing before testing by allowing the observer to adjust the position of the image in one eye until it was aligned with the image presented to the other eye. The alignment of the images seen by each eye will only work over a limited range. It would need to be supplemented by a prismatic correction in cases of larger deviations. The HMD was driven by a MAC laptop with an NVIDEA graphs card (GeForce 9400M, Santa Clara, CA).
One of the advantages of using an OLED display is that, unlike a Liquid crystal display (LCD), its luminance response is linear, and therefore gamma correction is not necessary. This also means that an 8-bit intensity range is available to encode contrast if the luminance is optimally adjusted, which provides adequate contrast resolution for this task. The calibration curves obtained with our Z800 dual pro goggles are displayed in Fig. 2. They were measured with a United Detector Technology photometer with a Vλ filter (i.e., the human luminosity function). The two screens' responses are identical except for a vertical displacement, that is, they differ only in their absolute luminance. There are two buttons on the controller box of the Z800 that allow for changes in mean luminance to be made independently for each screen, and it is important for dichoptic comparisons of sensitivity that the two screens are at the same mean luminance. This is best verified using a photometer.
Global motion stimuli were composed of arrays of moving dots (i.e., translational random dot kinematograms) presented within the two screens of a HMD. Each screen subtended 30° × 40°, and to aid binocular fusion, each circular display region (diameter, 22.2°) was surrounded by a binocular rectangular frame. The distance between the screens was adjusted to suit the interpupillary distance of each subject, and the vertex distance was also adjustable such that spectacles could be worn with the HMD. One hundred dots (each diameter 0.5°) were presented on a homogenous mid-gray background (mean luminance of 100 cd/m2) that filled the entire circular display window. The luminance modulation (Michelson contrast) and, hence, the visibility of the dots could be varied by increasing the luminance of the dots, with respect to the background, according to the following equation:
where Ldots and Lbackground are the dot and background luminance, respectively. The stimuli were composed of “signal dots” (left panel of Fig. 3), all which traveled in the same direction (leftward or rightward), and “noise dots” (middle panel of Fig. 3) in which each dot traveled in a random direction. During suppression measurements, the signal dots were viewed by one eye and the noise dots by the other (i.e., dichoptic viewing, right panel of Fig. 3). When the number of signal dots presented to one eye was decreased, the number of noise dots presented to the other eye was increased and vice versa so that the total number of dots seen by the participant was always 100. To discourage tracking of individual signal dots, each dot had a 5% probability of disappearing on each presentation frame, a manipulation known as limited lifetime. When a dot disappeared, a new dot immediately appeared at a random location. Stimuli were programmed in Matlab (Mathworks) using the psychophysics toolbox.9,10
The psychophysical technique that we have developed to measure suppression is based on a well-established visual stimulus known as a random dot kinematogram. Our stimulus is composed of a total of 100 moving dots (signal + noise) with one group of dots all moving in the same direction (the “signal direction”) and the other group of dots moving in random directions. We refer to these as the signal group and the noise group, respectively. The two groups are presented simultaneously, and the observer must judge the motion direction of the signal dots. The task is made more difficult by changing the proportion of signal to noise dots whereas the total number of dots remains constant. The ratio of signal to noise dots that represents the observer's threshold for correct identification of the motion direction of the embedded signal elements is called the motion coherence threshold. Our manipulation is to present the two groups of dots to different eyes. Therefore, in a binocularly normal individual, the noise seen by one eye makes the detection of the motion direction of the signal elements seen by the other eye more difficult.11,12 However, for the case of balanced binocular vision, it does not matter which eye sees the signal and which sees the noise. There is a “dichoptic balance” in the threshold performance in normal subjects. In amblyopes with suppression, it matters which eye sees the signal and which eye sees the noise. For example, if the fellow fixing eye sees the signal and the amblyopic eye sees the noise, then owing to the suppression of the amblyopic eye by the fellow fixing eye, performance will be at ceiling. On the other hand, if the amblyopic eye sees the signal and the fellow fixing eye sees the noise, then performance will be at chance. Thus, one would expect there to be an imbalance in the dichoptic thresholds because of suppression. By suitably imbalancing the contrast of the stimuli (be it either signal or noise) seen by the fellow fixing eye, we found that balanced dichoptic performance could be obtained, reflecting the fact that information from the two eyes was now being combined binocularly.6 In other words, imbalancing the input to the amblyopic binocular visual system can result in a balanced output, namely normal binocular combination. The extent of the signal imbalance needed to achieve this balanced performance (termed the balance point) provides a measure of the degree of suppression.6
The global motion coherence level of the stimulus was manipulated by constraining a fixed proportion of signal dots on each image update to move coherently along a translational trajectory and the remaining noise dots to move in random directions. Motion coherence thresholds were measured using a single-interval, forced-choice direction-discrimination procedure. On each trial, observers were presented with a global motion stimulus in which the signal dots moved along a rightward or leftward trajectory. The observers' task was to identify whether the motion was leftward or rightward. Data collection was performed using a three-down one-up staircase procedure with a proportional step size of 50% before the first reversal and 25% thereafter. The staircase varied the proportion of signal dots present on each trial, according to the observer's recent response history. The staircase terminated after six reversals, and thresholds (79% correct performance) were taken as the mean of the last five reversals. Each threshold reported was based on the mean of at least five staircases. Between two and five, thresholds were measured for each of a number of different interocular contrast ratios (reductions in contrast for the stimuli viewed by the fixing eye), one in which signal was presented to the fixing eye and noise to the amblyopic eye and vice versa. The luminance contrast for the fixing eye was varied (20, 40, 60, 80, and 100%) whereas that for the amblyopic eye was fixed to 100%. This is illustrated in Fig. 4A where dichoptic threshold ratio is plotted against the interocular contrast ratio. The solid arrows illustrate that a number of fixed contrast ratios were selected and the dichoptic threshold for each eye was measured for these contrast ratios (indicated by lines with double arrows) using interlaced staircases. In this way the balance point (i.e., the contrast ratio corresponding to balanced dichoptic performance—solid filled circular symbol) could be determined.
Before threshold measurement for the amblyopic observers, the square borders surrounding the stimulus display apertures were presented to each eye along with fixation dots in the center of the apertures flanked by nonius lines. Observers could use the arrow keys on the computer keyboard to move the position of the stimulus display aperture horizontally and vertically in the amblyopic eye until both apertures were aligned.
A second method was designed to speed up the previously described technique. In this method, the task was split into two parts. Part 1 was the measurement of a binocular motion coherence threshold where both eyes viewed the same stimulus that contained both signal and noise dots. Part 2 was the measurement of a dichoptic contrast threshold where signal was presented to the amblyopic eye and noise to the fellow eye. The number of signal dots presented to the amblyopic eye was based on the results of part 1. This method simplified what was previously described by fixing one parameter (the number of signal dots presented to the amblyopic eye) while measuring the other (the contrast of the noise presented to the fellow fixing eye that resulted in a coherence threshold). Specifically, we first determined the required number of signal dots under binocular viewing conditions at a fixed high contrast. We then used this threshold to fix the number of signal dots presented to the amblyopic eye at high contrast while varying the contrast of the noise dots in the fellow fixing eye to measure the point at which information was combined between the two eyes. This meant that rather than one long task including multiple interleaving staircases, the task could be split into multiple short staircases, which were then averaged. This is illustrated in Fig. 4B where dichoptic threshold ratio is plotted against the interocular contrast ratio. To determine the contrast ratio at which balanced dichoptic performance is obtained (corresponding to filled circular symbol), the number of signal elements that correspond to the coherence threshold for the fixing eye is first determined (binocular coherence threshold measure), and then with this number of signal elements presented to the amblyopic eye at a fixed high contrast, the contrast of noise presented to the fellow fixing eye is varied until a dichoptic coherence threshold is obtained (the contrast threshold measure). This is equivalent to working at a fixed balanced dichoptic threshold (solid arrow on ordinate in Fig. 4B) and varying the interocular contrast (indicated with line and double arrows in Fig. 4B) to determine the balance point (indicated by solid circular symbol).
The modification of the first, longer technique was based on the assumption that the number of signal dots required for task performance does not depend on whether the stimulus is presented binocularly (both eyes see both signal and noise) or dichoptically when the correct contrast imbalance is in place. This assumption is directly tested in the dataset from amblyopic participants presented below.
For binocular testing, the observers were first asked to align the screens as previously described. The task involved judging whether the dots were moving coherently to the right or to the left. However, rather than altering the signal to noise ratio in both eyes when also altering contrast, the binocular motion coherence threshold paradigm presented the same image (same signal to noise ratio) to each eye at a fixed contrast. Progressively, the binocular task became more difficult by increasing the proportion of noise dots until a threshold was reached using the same staircase parameters described for method 1 above. The results of five staircase measurements were then averaged to give a stable binocular motion coherence threshold. In the second task, the dots were presented dichoptically, and the signal to noise ratio was kept constant (based on the binocular measurement) while the contrast level was varied in the fellow fixing eye using a three-down one-up staircase technique. The staircase began with 0% contrast in the fellow fixing eye (i.e., no dots were visible), and contrast was increased in steps of 10% before the first reversal and 5% thereafter. Steps down in contrast were always 10% contrast. The staircase ran for six reversals, and the last five reversals were averaged to provide the threshold. The staircase converged on 79% correct performance. This was the point at which the noise dots presented to the fellow fixing eye were having the same effect on task performance under dichoptic conditions as they had under binocular conditions, indicating that normal binocular combination had taken place. One advantage of this method is that each threshold measurement takes only a few minutes, and depending on the reliability of those measurements, they may only need to be repeated three or four times. This can be compared with method 1, which takes up to 15 min for only one set of thresholds to be measured, a procedure that should be repeated at least three times.
Determining the Difficulty of the Psychophysical Task
Two difficulty levels were created depending on the ability of the individual's visual system to detect signal within noise. There were two versions of the task for both methods 1 and 2, with the same parameters altered. For the normal discrimination task, stimuli were shown for 1 s, and dots had a 5% chance of disappearing on a frame by frame basis. For subjects who were very good at detecting signal from noise dots, with good performance being defined as a motion coherence threshold of 5% signal dots or less, a harder version of the task was used. In the hard version, the stimuli were presented for 500 ms, and the probability of a dot disappearing on each frame was 50%. After participants were familiarized with the task, the first trial of each method determined which version of the program was used. All subsequent trials were completed using the same version—either normal or hard. If a subject completed the hard version on method 1, the same parameters were used for method 2.
Two observers with normal monocular and binocular vision and nine amblyopic observers completed methods 1 and 2 measurements. The clinical details of the amblyopic observers are given in Table 1.
A variety of clinical measurements and the psychophysical task described above were completed for each amblyopic participant. Clinical measurements included high and low contrast letter acuity (Bailey-Lovie Chart), grating acuity, and stereoacuity using the Frisby (Clement Clarke Int, Harlow, United Kingdom), TNO (Lameris Ootech B.V, Nieuwegein, The Netherlands), and Randot (Stereo Optical, Chicago, IL) tests. Standard clinical tests of suppression were also measured using distance and near Worth 4 light and Bagolini lenses. All observers wore their best optical correction during testing. Where habitual correction did not provide best-corrected acuity, a trial frame or contact lenses were used. Vision (uncorrected), visual acuity (corrected), refraction, suppression, and stereoacuity measurements are detailed in Table 1. The study was approved by institutional ethics committees, and all study protocols were in accordance with the Declaration of Helsinki.
Measurements of dichoptic performance using the global motion stimulus with the HMD are shown in Fig. 5 for two binocularly normal individuals. Following on from our earlier work on normal subjects11,13 and amblyopes,6 we computed the dichoptic threshold ratio for every contrast difference tested. The dichoptic threshold ratio is defined as the motion coherence threshold for signal dot presentation to the amblyopic eye divided by the motion coherence threshold for signal dot presentation to the fellow eye. Larger ratios indicate stronger suppression of the amblyopic eye. This is plotted against the contrast of the stimulus seen by the fellow eye. In a binocularly normal individual when both eyes see the same contrast (i.e., contrast of 100% in felloe fixing eye or FFE), it does not matter which eye sees the signal and which eye sees the noise because the two eyes are in “balance” (i.e., a dichoptic ratio of 1). As the contrast is reduced to one eye, the dichoptic performance ratio becomes imbalanced because now it does matter which eye sees the signal and which eye sees the noise because one eye has been put at a contrast disadvantage (i.e., the dichoptic performance ratio becomes <1). These expectations are realized in the data in Fig. 5, the best fitting line through the data on these coordinates intersects the horizontal line (indicating identical dichoptic performance at a contrast nearly 80 to 100%), which is the fixed contrast shown to one eye. The interocular contrast ratio that corresponds to the dichoptic performance ratio of 1 (i.e., where the best fitting line to the data intersects the horizontal dotted line passing through a dichoptic ratio of 1) is called the “balance point” and represents the contrast conditions under which balanced binocular performance is obtained, in other words, the point at which the visual system is combining information between the two eyes in a normally balanced fashion.
Another way of representing the same data, and one we now prefer to use, is to plot and fit the data for each eye separately; this is shown in the lower frames of Fig. 5. This allows separate assessment of the data from each eye that went into the computation of the dichoptic ratio measure described above. Here, one can see that as the contrast to one eye is reduced, its performance declines (i.e., coherence threshold increases) because the signal from that eye, let us say the right eye, is now of lower contrast than the noise from the left eye. Similarly, the performance of the left eye increases with contrast reduction to the right eye for the opposite reason. The two lines intersect at the balance point that is at the contrast where it does not matter which eye sees the noise and which eye sees the signal. The balance point is around 80 to 100% contrast because the other eye's contrast is fixed at 100%. Ratios can be noisy, and we, therefore, feel it is best to compare the results of each eye separately, as described.
Fig. 6 shows the results for the nine amblyopic subjects, who represent a range of amblyopia etiologies. These amblyopes also have a range of monocular acuities and levels of suppression. We measured dichoptic motion coherence performance as a function of the contrast reduction (the contrast in the amblyopic eye is fixed at 100%, and so by reducing the contrast in the fellow eye, we are changing the interocular contrast ratio, the parameter that was measured at a number of fixed levels in method 1: Fig. 5) shown to the fixing eye to see how much the contrast had to be reduced to the fixing eye before balanced binocular performance was achieved. This provides a quantitative measure of the degree of suppression. Measurements were repeated five times and we plot the average (±SE). The results are plotted such that the individual threshold for each eye can be assessed. We fitted linear functions to the average data for each eye and derived the balance point where these functions intersect. For some subjects such as RO, the balance point falls within the normal range at around 80 to 100%, meaning that balanced performance was obtained when the contrast to the fixing eye was almost the same as that seen by the amblyopic eye, in other words, there was virtually no suppression. The results for other subjects such as RS are very different. The contrast of the stimuli shown to the fixing eye had to be reduced to about 20% for a balance in performance to be found. In cases such as this, it is best to rerun the test at a lower range of contrasts so that the determination of the balance point falls within the test range. Accordingly, after an initial run with contrast levels of 100, 80, 60, 40, and 20%, contrast levels were then altered for all subjects to more specifically refine the balance point. The results were then averaged across all contrast levels tested, and an average balance point and contrast ratio intercept were calculated. It is worth noting that method 2 avoids the need for preselecting the contrast imbalances to test, therefore making the technique more efficient. The results for subject QM and PB need special mention as no balance point was found for the initial contrast range tested. It is clear from the pattern of the results in these cases of profound suppression that a much lower contrast range needs to be evaluated (corresponding to a large interocular contrast ratio).
Method 2 was also completed on the nine amblyopic subjects described above. Five trials were run and averaged for both the binocular motion coherence threshold and dichoptic contrast measurements. All subjects were able to complete the measurements and showed binocular combination. Methods 1 and 2 both provide a measurement of the number of signal dots required in relation to noise dots to correctly identify the direction of motion. Both methods also give a contrast level at which the thresholds are balanced, i.e., the percentage contrast that is required by the fellow eye to allow the equal motion coherence thresholds that are indicative of binocular combination. It was important to verify that the faster technique used in method 2 agreed with method 1, as the dots were presented binocularly and the assumption of a constant motion coherence threshold across viewing conditions had been made (as described above).
Comparisons between the two methods for these parameters are shown in Fig. 7. It can be seen that the two methods give comparable results for motion coherence thresholds (Fig. 7A) and contrast imbalance (Fig. 7B). The results shown in Fig. 7A were not significantly different between the two methods (p = 0.911), and the results in Fig. 7B demonstrated a significant correlation between methods 1 and 2 for the amblyopic subjects (p = 0.006). Both comparisons (dot thresholds and contrast levels) showed no significant differences on paired t-tests (p > 0.05). This was particularly important for the motion coherence thresholds as it supports the assumption underpinning method 2 that the motion coherence threshold remains constant between binocular viewing and contrast balanced dichoptic viewing.
A new technique is described that allows objective measurement of the degree of interocular suppression as a first step to its treatment.7,8 We have translated our initial approach in the laboratory6 to the clinic by using a calibrated HMD (Z800, OLED goggles). This provides a method with scientific foundations6 that can be used conveniently in the clinic where space is a concern. Currently, our goggles are driven by a laptop computer, but, in principle, this could be further miniaturized, and we are currently working to achieve this.
The first method described involves the measurement of motion coherence thresholds where signal dots are presented to one eye and noise dots to the other. The contrast of the fixing eye is reduced to the point where performance balances (where it does not matter which eye sees signal and which eye sees noise) between the eyes. This balance point represents conditions where the information is now being combined between the two eyes as it would be for a binocularly normal observer. That is, at the balance point, the information conveyed by the amblyopic eye is no longer being suppressed by the fellow fixing eye and is being binocularly combined. As such, the viewing conditions that allow this combination to take place not only provides a quantitative measure of suppression, something we do not have presently in the clinic, but also establishes ideal conditions for binocular training to reduce the suppression.7,8 Under these artificial conditions (i.e., where the two eyes see different contrasts), information is being combined by the two eyes of amblyopic observers for the first time. Repeated measurements under these conditions (i.e., binocular training) has been shown to reduce suppression and reestablish stereoscopic function in adults well past the so-called critical period7,8 and, therefore, holds great promise if applied to the younger age group. A concomitant improvement in monocular acuity of the amblyopic eye has been shown to follow reduction of suppression,7,8 suggesting that a significant fraction of the loss of acuity in adult amblyopes is because of active suppression, another reason why suppression needs to be measured and treated.
We have also described a modification of the previously reported psychophysical technique, which allows for a faster estimation of suppression strength. This technique allows one parameter to be fixed while another is measured, e.g., either the motion coherence threshold or the contrast imbalance. We have shown that the two methods give correlated results across a number of amblyopic observers. This was an important finding as it validates the use of the new technique.
So far, we have limited our measurement to adults, but there is no reason why the technique cannot be applied to a younger age group, particularly now that we have incorporated a faster measurement technique, which also allows breaks in between trials. The new task has been shortened to blocks of trials of approximately 3 min duration (the time to measure one contrast ratio), and it simply involves subjects determining whether the array of stimulus dots moves left or right. In other words, there is no significant cognitive aspect that would preclude younger children at least in the age group above 5 years. We are currently investigating the best way to make such measurements in the younger age group because the measurement and treatment of suppression may well be more relevant for children within the critical period than it is for adults well beyond it. One possibility is to add auditory or colored visual feedback within the goggles to reinforce correct responses.
This work was supported by a University of Auckland FRDF grant awarded to BT and JB and a CIHR POP grant to RFH. JB was supported by a University of Auckland Faculty Development Research Fund award.
Robert F. Hess
Department of Ophthalmology
McGill University, 687 Pine Avenue West, Room H4-14
Montreal, Quebec, Canada H3A 1A1
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Keywords:© 2011 American Academy of Optometry
suppression; amblyopia; strabismus; binocular vision