November 1999
Volume 40, Issue 12
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Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   November 1999
Binocular Depth-from-Motion in Infantile and Late-Onset Esotropia Patients with Poor Stereopsis
Author Affiliations
  • Manami Maeda
    From the Department of Ophthalmology, Nagoya University School of Medicine, Nagoya, Japan; and the
  • Miho Sato
    From the Department of Ophthalmology, Nagoya University School of Medicine, Nagoya, Japan; and the
  • Tomohisa Ohmura
    From the Department of Ophthalmology, Nagoya University School of Medicine, Nagoya, Japan; and the
  • Yoji Miyazaki
    From the Department of Ophthalmology, Nagoya University School of Medicine, Nagoya, Japan; and the
  • Ai–Hou Wang
    Department of Ophthalmology, College of Medicine, National Taiwan University, Taipei, Taiwan.
  • Shinobu Awaya
    From the Department of Ophthalmology, Nagoya University School of Medicine, Nagoya, Japan; and the
Investigative Ophthalmology & Visual Science November 1999, Vol.40, 3031-3036. doi:https://doi.org/
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      Manami Maeda, Miho Sato, Tomohisa Ohmura, Yoji Miyazaki, Ai–Hou Wang, Shinobu Awaya; Binocular Depth-from-Motion in Infantile and Late-Onset Esotropia Patients with Poor Stereopsis. Invest. Ophthalmol. Vis. Sci. 1999;40(12):3031-3036. doi: https://doi.org/.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

purpose. There are at least two possible ways to detect motion-in-depth binocular without monocular cues: the binocular disparities at different times and a mechanism that detects interocular velocity differences. The perception of interocular velocity differences (Binocular depth-from-motion [BDFM]) depends on the relative velocity of the images on the retina of the left and right eyes, and this information can be experienced by normal and some strabismic patients. The purpose of this study was to determine the characteristics of esotropic patients who have BDFM but have poor stereopsis.

methods. Forty-one infantile and 28 late-onset esotropia patients with poor stereopsis were studied. Dynamic stereopsis and BDFM were tested with computer-generated random dot stereograms and kinematograms. The correlations between BDFM and other binocular functional tests were determined.

results. A total of 31 (44.9%) patients, 15 (36.5%) of the infantile and 16 (57.1%) of the late-onset esotropia group, passed the BDFM test. None of these patients passed the random dot stereo test under static or dynamic conditions. Fusion of the Worth four dot test at near 0.3 m was correlated with the presence of BDFM. Three of the 15 infantile and 10 of the 16 late-onset esotropic patients with positive BDFM showed gross stereopsis as measured by the Titmus Fly. The angle of strabismus was significantly smaller in the patients with positive BDFM for the infantile and the late-onset esotropia groups.

conclusions. BDFM was present in about half of the esotropic patients who do not have fine stereopsis. Ocular alignment within 10 to 15 prism diopters is an important factor in obtaining BDFM. Strabismus surgery still provides some binocular benefit for infantile esotropia patients who were bypassed for early surgery. Separate mechanisms may underlie static stereopsis and BDFM.

Static stereopsis, which arises from the disparity of the retinal images on the two retinas, gives rise to the finest depth perception. To obtain a high level of stereopsis, good ocular alignment is essential,; therefore, obtaining or regaining good ocular alignment is one of the important goals for strabismus treatment. 
In strabismus clinics, conventional static stereopsis is routinely examined, but dynamic stereopsis, which requires expensive and space-occupying equipment, has not been routinely used. Fusion and stereopsis are considered to be static depth perception processes, which comes from the retinal disparity of the binocular images. However, in a dynamic world, the retinal images are always in motion, and there are both monocular and binocular depth cues from the motion. Monocularly, objects moving in depth result in changing retinal image size and motion parallax. There are at least two possible ways to detect motion-in-depth binoculary without monocular cues: the binocular disparities at different times and a mechanism that detects inter-ocular velocity differences. The perception of interocular velocity differences (binocular depth-from-motion [BDFM]) depends on the relative velocity of the images on the retina of the left and right eyes, and this information can be experienced by normal and some strabismic patients 1 (Fig. 1) . For objects moving in the real world, interocular velocity differences occur at the same time as changes in binocular disparity. Kitaoji and Toyama 2 reported that motion stereopsis can be preserved in patients with small angle strabismus who do not have static stereopsis. Thus, testing for the presence of binocular motion-in-depth in a clinical setting and learning the prerequisites for BDFM perception can provide important information to assess the visual capabilities of strabismic patients. 
One of the authors (AHW) has developed a computer program 3 that generates dynamic random-dot stereograms. In this program, disparity and motion cues can be included or omitted independently. We have tested patients with either early- or late-onset esotropia with this program to see whether BDFM was present despite the absence of static stereopsis. 
Methods
This study was performed in the Department of Ophthalmology of Nagoya University between December 1996 and December 1997. 
Controls
We examined 12 normal subjects (age, 26–30 years, 6 men and 6 women) without any ocular abnormality other than refractive errors (visual acuity; better than 20/20) to determine the normal responses and to select the optimal testing conditions. 
Esotropia Patients
Informed consent was obtained from the subjects or their guardians, and all procedures were conducted in accordance with the principles embodied in the Declaration of Helsinki. 
Forty-one patients with infantile esotropia and 28 with late-onset esotropia were examined. The patients in both groups showed worse than 3000 seconds arc. stereopsis as determined by the large Fly (+) in the Titmus Stereo Test. Patients with infantile esotropia were defined as those: whose esotropia was diagnosed before 6 months of age by an ophthalmologist or was confirmed by photographs; whose deviation was not abolished by a hyperopic correction; who had no central nervous system disorders or developmental delay; and who were born after 37 weeks of gestation. Late-onset esotropia was defined as an accommodative or partially accommodative esotropia with hyperopia, which became manifest after 18 months of age. Patients with paralytic esotropia, esotropia from organic disorders, premature birth (gestation before 37 weeks), and developmentally delayed children were excluded. The mean age at the time of examination was 8.8 years (age range, 4–19 years) for the infantile esotropic group and 13.1 years (age range, 5–31 years) for the late-onset esotropic group. 
Visual Stimulator
The computer program was run on a FMV-5100D4 computer (FUJITSU, Tokyo, Japan) and displayed on a 17-inch CRT in a dimly lit room. Anaglyphic random-dot stereograms and kinematograms were made up of red and green random-dots. The size of the screen was 31.0 × 22.0 cm with 320 × 200 pixels. When viewed at a 55.5-cm distance, each pixel subtended 360 second-arc. Four rectangles of 60 × 50 pixels (6° × 5° arc) were displayed on the monitor, and one was programmed to provide a depth cue. Throughout the testing session, the background was made up of a stable random-dot pattern with the same density as the 4 rectangles. 
The pair of rectangles seen by right and left eyes, t1R and t1L, was called a stereogram pair if they had the same random-dot pattern and included a disparity cue. If the rectangles were different and therefore had no motion cue, they were called a temporal correlogram. The rectangles seen by the same eye, t1R and t2R, were called kinematograms if they had the same random-dot texture and had cues for apparent motion. If the rectangles were different and therefore had no motion cues, they were called a temporal correlogram. In the kinematogram pair, if the rectangles moved in opposite directions, the fused target invoked a depth sensation (i.e., a movement in depth) in normal subjects. 
Test 1 was designed to test binocular motion-in-depth elicited by interocular disparity cues and/or BDFM elicited by movement cues. For this, t1L, t1R, t2L, and t2R were made up of the same random-dot pattern. Test 2 was designed to test only stereopsis, and t1R = t1L, but t1R and t1L were different from t2R and t2L. When the program is stopped, only one rectangle with a disparity of 360 second–arc is seen in depth by normal subjects, but no depth is seen by stereo blind subjects. Test 3 tested only BDFM without disparity cues, and t1R was different from t1L; however, t1R and t1L had the same pattern as t2R and t2L, respectively. The other three rectangles were seen by both eyes and were designed to move in the same directions. When the program is paused, four indistinguishable rectangles are seen by normal subjects, and no rectangles can be seen in depth by stereo blind subjects (Fig. 2)
Each patient sat facing the screen at 55.5-cm distance with a green filter on the right eye and red filter in front of the left eye. The computer randomly determined which one of the four rectangles would provide a depth cue. The subjects were asked to select the figure that appeared to move back and forth in the “Z” direction. For control, we occluded one eye or paused the program (Test 3) during the course of the tests to be certain that answers were based on disparity or motion cues. The correct answer was given to the patients immediately after each test. The test was repeated 10 times in a forced-choice manner, and a passing score was set at eight correct answers. After the subject passed Test 1, Tests 2 and 3 were conducted. If a subject passed both Tests 1 and 2, he/she was designated as having stereopsis from disparity. If the subject passed both Tests 1 and 3, but not Test 2, he or she was defined as having BDFM-positive without stereopsis. 
Testing Methods
Controls.
All three tests were first performed on the normal subjects. Test 1 and Test 2 were performed on control subjects. Test 3 was performed with various range of movement and with different velocities of the random-dot pattern to determine the optimal stimulus conditions. The range and speed that allowed the control subjects to detect the depth most easily were selected as the testing condition for the esotropic patients. To determine the minimum visual acuity necessary to pass the BDFM test, we blurred the vision in one or both eyes with Einschleich occlusion partielle filters (Ryser Optik, Basel, Germany) and conducted Tests 1, 2, and 3 on 5 normal patients. In addition, to verify that this test can be passed by horizontal disparity but not by flickering or odd sensation, we tested with 3 normal subjects by rotating the monitor 90°. 
Esotropic Subjects.
We performed complete ophthalmic examinations including visual acuity, Titmus Stereo tests, TNO stereo test, Bagolini striated lenses test, and Worth four-dot test at near (0.3 m) and distance (5 m) on all the subjects. The angle of strabismus was measured by simultaneous prism cover test at near and far. 
Data Analysis
The differences between the patients having BDFM (BDFM+) and those lacking BDFM (BDFM−) were analyzed statistically with either the chi-square test or Mann–Whitney test, and P < 0.05 was accepted as statistically significant. 
Results
Normal Subjects
The results obtained from the normal subjects showed that the optimal repetition rate and range of movement of the two targets was 3.5 Hz and 1 pixel, respectively. All normal subjects perceived a depth sensation on all tests. When the visual acuity was artificially reduced to 16/20 or better, no control subjects failed Test 3. However, they also reported that they felt depth sensation more strongly on Tests 1 and 2 than Test 3. No one passed any tests when the monitor was rotated 90°. 
Patients with Esotropia
The relationship between BDFM and the sensory tests is shown in Table 1 . None of the patients passed Test 2 regardless of the time of onset of the ocular deviation (i.e., none had stereopsis). Fifteen (36.5%) patients in the infantile group and 16 (57.1%) in the late-onset group (total = 31, 44.9%) passed Tests 1 and 3 but not 2 and were classified as having positive BDFM without stereopsis. Of the other 38 patients, 26 in the infantile group and 12 in the late-onset group did not pass any test. There was no statistical difference between early-onset esotropia and late-onset esotropia in the incidence of positive BDFM. 
The distribution of the angle of deviation at near for the infantile esotropia and the late-onset esotropia groups is shown in Figures 3 A and 3B, respectively. The patients with positive BDFM (black squares) had significantly smaller angles of deviation (infantile onset, 4.33 SD, 5.68 prism diopters [pd]; late-onset, 8.00 SD, 6.65 pd) than the patients lacking BDFM (infantile-onset, 12.2 SD, 2.46 pd; late-onset, 18.4 SD, 9.00 pd; P = 0.0016; Mann–Whitney test). There was no statistical difference between the age at the time of examination and the presence of BDFM in both groups (infantile-onset, P = 0.205; late-onset, P = 0.0885 Mann–Whitney test). Of the 41 infantile esotropia patients, 36 had undergone strabismus surgery at a mean age of 49.8 months with a (range, 25–120 months). Of the 28 late-onset esotropia patients, 10 patients had undergone strabismus surgery at a mean age of 166 months (range, 24–356 months). There was no statistical difference between the presence of BDFM and whether the patient had undergone surgery. In addition, there was no statistical difference between a positive BDFM and the age at the time of surgery in both groups (infantile-onset, P = 0.796; late-onset, P = 0.317 Mann–Whitney test). 
There was a high correlation between a positive Titmus Fly test and a positive BDFM (P = 0.0009, chi-square test). None of the patients passed Plate I of the TNO stereo test. Fusion of the Worth four-dot test at 0.3 m and positive BDFM were highly correlated (P < 0.0001, chi-square test). There was a significantly higher number of patients with BDFM who were able to fuse the Worth four-dot test at 0.3 m. None of the patients fused the Worth four-dot test at 5 meters. There was no correlation between suppression under Bagolini striated lenses test and BDFM and also no correlation between the visual acuity and the presence of BDFM. 
Discussion
In this study, we tested whether binocular detection of motion-in-depth, which is evoked by the simultaneous nasal and temporal shift of the retinal images in the two eyes, was present in patients with infantile and late-onset esotropia. We found that 18 of the 31 subjects who did not have stereopsis as determined by the Titmus fly test, showed binocular detection of motion-in-depth sensation. Removing the disparity cues from the visual stimulus did not interfere with their depth perception but removing motion cues from the visual stimulus completely blocked their depth judgment. This latter fact was verified by the absence of disparity sensors as tested by static stereopsis test. When one eye was occluded, none of the subjects could pass the BDFM test. We also rotated the monitor screen 90° to give a vertical directional movement of the targets and no depth sensation was evoked. These findings indicate that the binocular depth perception came solely from inter-ocular velocity differences in the horizontal direction. 
In contrast, control subjects answered that they felt stronger depth sensation with Tests 1 and 2 than Test 3, which means they rely on interocular disparity cue rather than interocular velocity cue. This finding is supported by the study of Halpen, 4 who examined the quality of motion-in-depth from interocularly uncorrelated motion-defined forms and concluded that the perceived magnitude of depth is less than that seen with interocularly correlated targets. Cumming and Parker 5 reported that motion-in-depth is primarily detected by means of temporal changes in binocular disparity and that interocular velocity differences play a minor role, if any, in normal subjects. Our finding suggests that the subjects had grown up without the experience of interocular disparity perception, interocular velocity differences could play some role for motion-in-depth sensation. 
The angle of the strabismus measured by simultaneous prism cover test, fusion of the Worth four-dot test at near, and the existence of gross stereopsis were factors that were correlated with the presence of positive BDFM. The possible reason for the strong correlation between the Worth four-dot test at near and BDFM is related to the size of the stimulus and the technique used in the computer program for binocular separation. The subtense of the Worth four-dot test at 5 m is 0.5° and that at 0.3 m is 6°, which is the same as the horizontal size of each rectangle of the BDFM test. Therefore, patients with peripheral fusion are probably good candidates for positive BDFM. The Bagolini striated test, on the other hand, was not correlated with BDFM. If the BDFM had been tested under different conditions of binocular separation, the results might have been different. 
Kitaoji and Toyama 2 reported earlier that motion stereopsis can be preserved in strabismic patients and that the existing strabismus angle was an important factor related to motion perception. In our computer-generated patterns, the movement of the images was not as smooth as that shown by a galvanometer because of the nature of computer graphic generation. When the image movement is too large, or too slow, or too fast, the sensation of continuous movement is not elicited. Because of the faster movement of the images, 3.5 Hz, compared with the 1 Hz used by Kitaoji and Toyama, 2 it was not possible to verify whether the approaching and receding phases were correctly identified. However, the subjects with BDFM clearly stated that they perceived a back and forth movement. Some of the esotropic patients pointed out that the range of movement varies on each individual. 
This study verified that the patients without good binocularity under static conditions, such as infantile esotropia patients, can obtain or regain a different kind of binocularity under dynamic conditions. Interestingly, infantile-onset esotropia patients in this study were all aligned after age two, and the age at surgery did not interfere with the success rate of the BDFM test. This finding is supported by the fact that the plasticity of the motion pathway remains“ soft-wired” longer than the critical period for fine stereopsis in humans. 6  
It has been established that the peripheral retina is more sensitive to motion and that motion is transmitted to the middle temporal area (MT), where almost all neurons are directionally selective. Direction and orientation selectivity of neurons in visual are in the MT of the macaque. 7 The detection and analysis of motion may also be required in conjunction with the depth perception. Bradley et al. reported the existence of an important link between disparity and transparent motion detection in MT and suggested that binocular disparity in MT may facilitate velocity processing. 8 Recently, MT is reported to be important for the perception of structure-from-motion. 9 Thus, BDFM that comes from binocular detection of velocity could be helpful in the perception of motion-in-depth and structure-from-motion with strabismic patients who lack disparity perception. 
Conclusions
BDFM was present in more than half of the esotropic patients who do not have fine stereopsis. Ocular alignment within 10 to 15 prism diopters is an important factor in obtaining BDFM. Strabismus surgery still provides some binocular benefit for infantile esotropia patients who were bypassed for early surgery. Separate mechanisms may underlie static stereopsis and BDFM. 
 
Figure 1.
 
Diagram of the movement of retinal images with the movement of a target. (A) The retinal images move in opposite directions to give a depth sensation. (B) The retinal images move in the same direction and give no cue for depth sensation.
Figure 1.
 
Diagram of the movement of retinal images with the movement of a target. (A) The retinal images move in opposite directions to give a depth sensation. (B) The retinal images move in the same direction and give no cue for depth sensation.
Figure 2.
 
(A) Test 1 dynamic stereopsis and BDFM. In one rectangle, the same random dots include disparity cues moving in opposite directions for the two eyes. (B) Test 2 dynamic stereopsis. In one rectangle, the same random dots include disparity cues moving in the same direction and no motion cue is included. (C) Test 3 BDFM. In one rectangle, the random dots move in opposite directions for the two eyes.
Figure 2.
 
(A) Test 1 dynamic stereopsis and BDFM. In one rectangle, the same random dots include disparity cues moving in opposite directions for the two eyes. (B) Test 2 dynamic stereopsis. In one rectangle, the same random dots include disparity cues moving in the same direction and no motion cue is included. (C) Test 3 BDFM. In one rectangle, the random dots move in opposite directions for the two eyes.
Table 1.
 
Comparative Data between BDFM and Conventional Binocular Tests (Chi-Square Test)
Table 1.
 
Comparative Data between BDFM and Conventional Binocular Tests (Chi-Square Test)
BDFM(+) n = 31 BDFM(−) n = 38 Chi-Square Test
Titmus stereo tests
Fly(+) 13 3 P = 0.0009
Fly(−) 18 35
Worth four-dot test at 0.3 m
Fusion(+) 29 11 P < 0.0001
Fusion(−) 2 27
Bagolini striated lenses test
SUP(+) 14 21 NS
SUP(−) 17 17
Figure 3.
 
(A) Present angle of strabismus and BDFM (infantile esotropia). (B) Present angle of strabismus and BDFM (late-onset esotropia).
Figure 3.
 
(A) Present angle of strabismus and BDFM (infantile esotropia). (B) Present angle of strabismus and BDFM (late-onset esotropia).
The authors thank Professor Yozo Miyake for his continuous encouragement during the course of this study. 
Beverley KI, Regan D. Evidence for the existence of neural mechanisms selectively sensitive to the direction of movement in depth. J Physiol. 1973;235:17–29. [CrossRef] [PubMed]
Kitaoji H, Toyama K. Preservation of position and motion stereopsis in strabismus. Invest Ophthalmol Vis Sci. 1987;28:1260–1267. [PubMed]
Wang A–H. Binocular depth-from-motion versus depth from disparity of strabismic patients. Invest Ophthalmol Vis Sci Suppl. 1996;37((3))S1290.Abstract nr B193
Halpen DL. Stereopsis from motion defined contours. Vision Res. 1991;31:1611–1617. [CrossRef] [PubMed]
Cumming BJ, Parker AJ. Binocular mechanisms for detecting motion-in-depth. Vision Res. 1994;34:483–495. [CrossRef] [PubMed]
Norcia AM, Hamer RD, Jampolsky A, Orel–Bixler D. Plasticity of human motion processing mechanisms following surgery for infantile esotropia. Vision Res. 1995;35:3279–3296. [CrossRef] [PubMed]
Albright TD. Direction and orientation selectivity of neurons in visual are MT of the macaque. J Neurophysiol. 1984;52:1106–1130. [PubMed]
Bradley DC, Quian N, Anderson AA. Integration of motion and stereopsis in middle temporal cortical area of macaques. Nature. 1995;373:609–611. [CrossRef] [PubMed]
Gregory C, Cumming BG, Newsome WT. Cortical area MT and the perception of stereoscopic depth. Nature. 1998;394:677–680. [CrossRef] [PubMed]
Figure 1.
 
Diagram of the movement of retinal images with the movement of a target. (A) The retinal images move in opposite directions to give a depth sensation. (B) The retinal images move in the same direction and give no cue for depth sensation.
Figure 1.
 
Diagram of the movement of retinal images with the movement of a target. (A) The retinal images move in opposite directions to give a depth sensation. (B) The retinal images move in the same direction and give no cue for depth sensation.
Figure 2.
 
(A) Test 1 dynamic stereopsis and BDFM. In one rectangle, the same random dots include disparity cues moving in opposite directions for the two eyes. (B) Test 2 dynamic stereopsis. In one rectangle, the same random dots include disparity cues moving in the same direction and no motion cue is included. (C) Test 3 BDFM. In one rectangle, the random dots move in opposite directions for the two eyes.
Figure 2.
 
(A) Test 1 dynamic stereopsis and BDFM. In one rectangle, the same random dots include disparity cues moving in opposite directions for the two eyes. (B) Test 2 dynamic stereopsis. In one rectangle, the same random dots include disparity cues moving in the same direction and no motion cue is included. (C) Test 3 BDFM. In one rectangle, the random dots move in opposite directions for the two eyes.
Figure 3.
 
(A) Present angle of strabismus and BDFM (infantile esotropia). (B) Present angle of strabismus and BDFM (late-onset esotropia).
Figure 3.
 
(A) Present angle of strabismus and BDFM (infantile esotropia). (B) Present angle of strabismus and BDFM (late-onset esotropia).
Table 1.
 
Comparative Data between BDFM and Conventional Binocular Tests (Chi-Square Test)
Table 1.
 
Comparative Data between BDFM and Conventional Binocular Tests (Chi-Square Test)
BDFM(+) n = 31 BDFM(−) n = 38 Chi-Square Test
Titmus stereo tests
Fly(+) 13 3 P = 0.0009
Fly(−) 18 35
Worth four-dot test at 0.3 m
Fusion(+) 29 11 P < 0.0001
Fusion(−) 2 27
Bagolini striated lenses test
SUP(+) 14 21 NS
SUP(−) 17 17
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