Listing's law in strabismus and amblyopia: a preliminary report

We investigated whether Listing's law applies in patients with diminished or no stereopsis due to strabismus or amblyopia. Eye movements of normal subjects and patients with strabismus and/or amblyopia were recorded during monocular and binocular fixation; from these data the shape and relative orientation of displacement planes were calculated. In normal subjects, monocular or binocular fixation did not influence the thickness and relative orientation of displacement planes. No differences were found between normals and the patient with amblyopia due to anisometropia. In one patient with strabismus but without amblyopia, the orientation of displacement planes depended on the fixation conditions; a coupling between horizontal vergence effort and plane orientation was observed. Patients with amblyopia and strabismus showed abnormally shaped and/or abnormally orientated displacement planes, which depended on the fixation conditions. Differences between both eyes in the shape of the planes were also observed. These results show that normal Listing behavior can be present in subjects with diminished stereopsis. They also show that normal stereopsis does not necessarily mean normal Listing behavior, suggesting that Listing's law is mainly a result of motor strategy.     

The influence of eye muscle surgery on shape and relative orientation of displacement planes: Indirect evidence for neural control of 3D eye movements

Is Listing's law a consequence of 2D control of eye positioning, where eye torsion is determined by the biomechanical properties of the orbit, or is it a reflection of full 3D neuronal control? This was investigated by observing the influence of a change in mechanical properties of the eye socket on 3D eye movements. The shape and relative orientation of displacement planes were measured using scleral search coils before and after operation of five patients with strabismus. The operation influenced the shape of displacement planes in both eyes of all patients. After the operation, most patients obeyed Listing's law more accurately: a monocular, surgically induced, orbital change caused binocular improvements of torsional control. The relative orientation of planes also changed, but no clear relationship was found between the type of operation and the direction of rotation. The results suggest that Listing's law is not just a result of the biomechanical properties of the eye socket, but has a neural basis.     

斜视弱视患者的双眼视觉状况及其矫治

本文在复习正常双眼视觉的概念及检查双眼视觉的常用方法和双眼视觉正常范围的基础上,介绍了单眼深度感知和双眼立体视觉近年来神经生理学及神经解剖学的研究进展,即单眼深度线索和双眼深度线索获得的深度感知在顶叶皮层的CIP区（顶尾侧）被整合,强调了单眼及双眼均可感知立体视觉。重点阐述斜视、弱视患者双眼单视及双眼立体视觉受到损害的状况,以及应用脱抑制训练、融合训练、立体视训练等方法矫治双眼视觉缺陷的结果。     

Increased drift in amblyopic eyes.

Reports are conflicting on the presence of increased drift in amblyopic eyes. Furthermore, the individual effects of either amblyopia or strabismus alone on ocular drift have not been systematically investigated. We therefore used a photoelectric method to record horizontal eye position during monocular and binocular fixation in patients having amblyopia without strabismus, intermittent strabismus, or constant strabismus amblyopia. Our principal finding was increased drift amplitude (up to 3.5 degree) and velocity (up to 3.0 degrees per second) in amblyopic eyes during monocular fixation. While increased drift was found 75% of the time in amblyopia without strabismus and 50% of the time in constant strabismus amblyopia, it was found only 20% of the time in intermittent strabismus. Amblyopic drift could be either error-producing or error-correcting in nature. Increased drift was not present during monocular fixation with the dominant eye or during binocular fixation in any of our 16 patients. We therefore conclude that amblyopia and not strabismus is a necessary condition for the presence of markedly increased fixational drift. Increased drift amplitude but not velocity may adversely affect visual acuity in the amblyopic eye.     

屈光参差性弱视与斜视性弱视临床疗效的比较

目的:分析比较屈光参差性与斜视性弱视的治疗效果。方法:前瞻性研究。2018-07/2020-01在我院门诊确诊的并首次接受治疗的单眼弱视患者46例,平均年龄9±3岁,其中男26例,女20例,按照临床诊断分为斜视性弱视组(无屈光不正),共23例,平均年龄9±3岁,其中男12例,女11例。以及屈光参差性弱视组,共23例,平均年龄9±3岁,其中男14例,女9例。对两组患者采用遮盖及精细训练治疗弱视,于治疗前及治疗后采用国际标准视力表检测视力、用Titmus图谱行立体视锐度的检测。比较两组患者经弱视治疗前后最佳矫正视力及立体视恢复的差异。结果:治疗前两组患者弱视眼的最佳矫正视力无差异(t=-0.475,P>0.05),但斜视性弱视患者的立体视功能明显低于屈光参差性弱视患者(t=-3.919,P<0.001);通过2mo的治疗,两组患者最佳矫正视力提高值有明显差异(t=-2.946,P<0.01),而两组患者立体视提高值无差异(t=1.305,P>0.05);通过6mo的治疗,两组患者最佳矫正视力提高差值有明显差异(t=-2.353,P<0.05),两组患者立体视提高差值也有明显差异(t=2.218,P<0.05);但在6mo时斜视性弱视患者的立体视水平仍低于屈光参差性弱视患者(t=-2.760,P<0.01)。结论:治疗前视力相同的斜视性弱视与屈光参差性弱视,斜视性弱视患者的立体视功能损伤更重。通过治疗,屈光参差性弱视患者的视力恢复较快,而斜视性弱视患者的立体视功能恢复较快,但其立体视功能水平仍低于屈光参差性弱视患者。     

Stereoacuity degradation by experimental and real monocular and binocular amblyopia

Fourteen normal adult volunteers with normal binocular single vision and normal stereoacuity submitted to monocular and binocular degradation of their stereoacuity by cycloplegia and fogging with spherical lenses. Stereoacuity (SA) was reduced as soon as visual acuity (VA), both monocular and binocular, was reduced. There was a marked similarity in the degree of SA reduction produced by monocular and binocular amblyopia. The degree of SA reduction was slightly more marked with monocular decrements than with binocular at VAs between 20/25 and 20/50. Significant intersubject variation was noted. The majority of subjects maintained gross SA at 20/200 monocular or binocular. One subject was reduced to gross stereopsis at 20/30 monocular and 20/50 binocular VAs. Two subjects were able to retain 40 sec of SA until vision was degraded to 20/50. Conversely, 40 sec of SA was not achieved by any subject at monocular or binocular vision less than 20/40 (test for malingering). Thirteen patients with real monocular and binocular organic or functional amblyopia were then compared with the experimental group. On the whole, patients scored somewhat better than normals but their scores fell within the range of responses found in the normal group.     

Binocular interactions in normal and anomalous binocular vision

Binocular interactions for grating patterns were investigated in humans with normal binocular vision and in humans with abnormal binocular visual experience due to strabismus and/or amblyopia via 1) comparison of monocular and binocular contrast thresholds; 2) interocular transfer of the threshold elevation aftereffect; and 3) dichoptic masking. Whereas the normal observers showed improved binocular over monocular contrast sensitivity (i.e., binocular summation) and substantial interocular transfer of the threshold elevation aftereffect, the abnormal observers showed an absence of binocular summation and no significant interocular transfer. The dichoptic masking experiments showed that a suprathreshold masking grating presented to one eye elevated the contrast threshold for gratings presented to the fellow eye, within a narrow range of spatial frequencies (about 1 octave wide at half height) and orientations, centered about the spatial frequency and orientation of the mask. The magnitude and bandwidth of this masking effect was similar in subjects with normal and abnormal binocular vision, occurring even when the masking grating was presented to the amblyopic eye. These effects depend upon the contrast of the masking grating. In individuals with normal binocular vision, a grating with subthreshold contrast presented to one eye reduces the contrast threshold for detection of gratings of similar spatial frequency and orientation presented to the fellow eye. No such subthreshold summation is evident in the amblyopic observers. We conclude that while strabismus and/or amblyopia disrupted the normal excitatory interactions between the two eyes, cortical inhibitory binocular connections were not disrupted.     

The influence of eye muscle surgery on shape and relative orientation of displacement planes: Indirect evidence for neural control of 3D eye movements

Is Listing's law a consequence of 2D control of eye positioning, where eye torsion is determined by the biomechanical properties of the orbit, or is it a reflection of full 3D neuronal control? This was investigated by observing the influence of a change in mechanical properties of the eye socket on 3D eye movements. The shape and relative orientation of displacement planes were measured using scleral search coils before and after operation of five patients with strabismus. The operation influenced the shape of displacement planes in both eyes of all patients. After the operation, most patients obeyed Listing's law more accurately: a monocular, surgically induced, orbital change caused binocular improvements of torsional control. The relative orientation of planes also changed, but no clear relationship was found between the type of operation and the direction of rotation. The results suggest that Listing's law is not just a result of the biomechanical properties of the eye socket, but has a neural basis.     

Fixational eye movements in amblyopia and strabismus

Horizontal eye position was monitored using a photoelectric method during monocular and binocular fixation in four patients having amblyopia without strabismus, thirteen patients having constant strabismus with amblyopia, and five patients having intermittent strabismus. Four abnormalities of fixation were found: increased drift, saccadic intrusions, manifest nystagmus, and latent nystagmus. Increased drift was related to the presence of amblyopia, while saccadic intrusions and nystagmus were related to the presence of strabismus. Understanding dynamic aspects of oculomotor control can provide insight into clinical assessment of fixation in amblyopia and strabismus.     

Abnormal saccadic substitution during small-amplitude pursuit tracking in amblyopic eyes.

Small-amplitude, low-velocity, predictable triangular tracking was tested in patients having amblyopia without strabismus, intermittent strabismus, or constant strabismus amblyopia by means of a photoelectric eye-movement recording technique. In the majority of amblyopic patients, abnormal saccadic substitution was found; that is, abnormally large saccades rather than small-amplitude smooth movements were used by the amblyopic eye to follow a spot stimulus that moved horizontally with low to high frequencies. Pursuit for the same range of stimuli was normal for binocular tracking and for monocular tracking with the dominant eye, pointing to a sensory rather than motor basis for the defect. This abnormal saccadic substitution response appeared to be related to the presence of amblyopia rather than strabismus. Several possible mechanisms responsible for causing this unusual response are discussed, including impairment of direction sense over small central regions of the amblyopic eye.     

斜视手术前后双眼单视注视野的临床研究

目的　研究不伴弱视的斜视患者术前、术后双眼单视注视野的变化 ,并对双眼单视注视野检查评价双眼单视功能的意义进行探讨。方法　 (1 )斜视患者术前及术后进行同视机和Titmus立体图检查。 (2 )利用Bagolini线状镜分离双眼 ,通过弧形视野计检查斜视患者术前、术后双眼单视注视野。 (3 )对照组进行同视机、Titmus立体图和双眼单视注视野检查。结果　 (1 )术前内斜视病人及恒定性外斜视病人检查无双眼单视注视野 ,间歇性外斜视病人控制正位时存在双眼单视注视野 ,但不稳定 ,其范围与对照组比较无差异 ,术后所有斜视病人双眼单视注视野均存在 ,其范围与对照组比较无差异。 (2 )双眼单视注视野检查结果与同视机、Titmus立体图所查斜视病人双眼单视功能结果相一致。结论　利用Bagolini线状镜和弧形视野计检查双眼单视注视野可以从心理物理学方面了解斜视病人术前、术后在日常生活中双眼单视功能情况。该方法经济 ,简便 ,易行。临床上这种方法与其他检查方法相结合可以更全面地了解斜视病人术前、术后双眼单视功能情况。     

Experience-expectant development of contour integration mechanisms in human visual cortex

Extended contours are a common feature of natural images. Most previous studies have considered contour integration as a two-dimensional process of linking like-oriented elements along their common orientation axis. Yet contours exist in a three-dimensional world, and one might therefore ask about the relationship between contour integration and binocular vision. Using an event-related potential assay of contour integration, we demonstrate that patients with strabismic amblyopia show a relative insensitivity to Gabor-defined contours in their dominant eyes, all of which had normal acuity. These deficits were not seen in the dominant eyes of patients with anisometropic amblyopia without strabismus, but were present in the amblyopic eyes of patients with either strabismus or anisometropia. Deficits were also found in both eyes of strabismus patients who had normal visual acuity in each eye, but who had strongly reduced or absent stereopsis. These results suggest that the maturation of contour detection mechanisms depends at least in part on the presence of normal binocular interaction during a developmental critical period.     

Latency of saccades, vergence, and combined movements in children with early onset convergent or divergent strabismus

The goal of this study was to examine latency of horizontal eye movements in the natural space (saccades, vergence, and combined saccade-vergence movements) in children with early onset convergent or divergent strabismus. Ten children were tested (8-11 years old): three with divergent strabismus, seven with convergent strabismus. A paradigm was used to elicit pure lateral saccades at far and near distance, pure vergence (convergence and divergence) and saccades combined with vergence movements. Horizontal eye movements from both eyes were recorded simultaneously by a photoelectric device (Oculometer, Dr. Bouis). The latency of saccades (at far and near distance), of vergence (convergence and divergence), and of combined movements greatly varies among subjects and has tendency to be longer than that observed in normal children of matched age, however, these differences reach significance in only a few cases. Children with divergent strabismus and residual gross binocular vision show abnormally longer vergence latencies than children with convergent strabismus without binocular vision. The initiation of combined movements does not show a dominant pattern, such as preceding vergence, as is found in normal children. Finally, strabismus surgery has no major effect on latencies. We conclude that there is no overall deficiency in latencies of eye movements in 3D space in children with early onset strabismus. Most likely, monocular visual input can be efficient as normal binocular vision for vergence movements. In a few subjects with divergent strabismus and fragile, intermittent binocular vision, latencies can be abnormally long, just because of the fragile binocular input and/or attention effort needs to use it. The absence of a pattern of initiation similar to normal children could be due to attention and fixation capabilities.     

屈光参差性弱视儿童视力与立体视的关系

目的探究相同屈光参差范围内不同类型屈光参差性弱视儿童的视力与立体视情况,以及视力、屈光参差类型对拥有立体视与否的影响。方法回顾性研究。收集56例屈光参差性弱视儿童和52例伴有斜视的屈光参差性弱视儿童以及20例正常儿童相应检查数据,检查包括矫正视力、屈光程度、随机点动态2阶粗糙立体视。采用多元方差分析3类儿童的视力差异,统计立体视分布情况,运用非条件logistic回归分析视力与屈光参差类型对拥有立体视与否的影响。结果单纯屈光参差性弱视儿童与伴有斜视的屈光参差性弱视儿童的视力差异无统计学意义（F=3.58,P=0.0314,校正α=0.016）。单纯及伴有斜视的屈光参差性弱视儿童粗糙立体视拥有率分别为96%,71%。在双眼视力一致的条件下,伴有斜视的屈光参差性弱视与单纯屈光参差性弱视儿童相比,拥有2阶立体视的OR估计值为0.132（95%CI：0.034~0.503）。在屈光参差类型一致的条件下,高、中双眼视力平衡度与低双眼视力平衡度相比,拥有2阶立体视的OR估计值分别为5.161（95%CI：0.868~30.675）和3.939（95%CI： 0.920~16.858）。结论相同屈光参差程度范围中不同类型屈光参差性弱视儿童的视力差异不明显;伴有斜视的屈光参差性弱视儿童立体视缺损的可能性更高,并且双眼不平衡度越高引起的立体视下降越明显。     

Binocular contrast summation and inhibition in amblyopia

The monocular contrast sensitivity loss in amblyopia is well documented. We investigated the influence of interocular sensitivity difference on binocular contrast sensitivity in amblyopia. Monocular and binocular contrast sensitivity functions of six amblyopes (three strabismic and three anisometropic) were measured. The monocular contrast sensitivity loss depended on the type of amblyope. Anisometropic amblyopes generally showed high frequency losses. Strabismic amblyopes showed losses at both low and high spatial frequencies. Binocular performance was assessed in terms of binocular ratios (binocular/non-amblyopic). A binocular ratio greater than 1 indicates binocular summation (binocular > monocular) while a ratio less than 1 shows binocular inhibition (binocular < monocular). In all subjects, the binocular ratio depended on the difference between the amblyopic and the non-amblyopic eye. Minimal interocular difference produced binocular summation, the magnitude of which decreased as the difference between the two eyes increased. Further increases in the monocular difference produced binocular inhibition. Anisometropic amblyopes showed a greater degree of binocular summation at low spatial frequencies compared to strabismic amblyopes. Both types of amblyopes showed binocular inhibition at high spatial frequencies. Clinical implications of binocular summation and inhibition in amblyopia are discussed.     

Suppression of metabolic activity caused by infantile strabismus and strabismic amblyopia in striate visual cortex of macaque monkeys.

INTRODUCTION: Suppression is a major sensorial abnormality in humans and monkeys with infantile strabismus. We previously reported evidence of metabolic suppression in the visual cortex of strabismic macaques, using the mitochondrial enzyme cytochrome oxidase as an anatomic label. The purpose of this study was to further elucidate alterations in cortical metabolic activity, with or without amblyopia. MATERIALS AND METHODS: Six macaque monkeys were used in the experiments (four strabismic and two control). Three of the strabismic monkeys had naturally occurring, infantile strabismus (two esotropic, one exotropic). The fourth strabismic monkey had infantile microesotropia induced by alternating monocular occlusion in the first months of life. Ocular motor behaviors and visual acuity were tested after infancy in each animal, and development of stereopsis was recorded during infancy in one strabismic and one control monkey. Ocular dominance columns (ODCs) of the striate visual cortex (area V1) were labeled using cytochrome oxidase (CO) histochemistry alone, or CO in conjunction with an anterograde tracer ([H 3 ]proline or WGA-HRP) injected into one eye. RESULTS: Each of the strabismic monkeys showed inequalities of metabolic activity in ODCs of opposite ocularity, visible as rows of lighter CO staining, corresponding to ODCs of lower metabolic activity, alternating with rows of darker CO staining, corresponding to ODCs of higher metabolic activity. In monkeys who had infantile strabismus and unilateral amblyopia, lower metabolic activity was found in (suppressed) ODCs driven by the nondominant eye in each hemisphere. In monkeys who had infantile esotropia and alternating fixation (no amblyopia), metabolic activity was lower in ODCs driven by the ipsilateral eye in each hemisphere. The suppression included a monocular core zone at the center of ODCs and binocular border zones at the boundaries of ODCs. This suppression was not evident in the monocular lamina of the LGN, indicating an intracortical rather than subcortical mechanism. CONCLUSION: Suppression of metabolic activity in ODCs of V1 differs depending upon whether infantile strabismus is alternating or occurs in conjunction with unilateral amblyopia. Our findings reinforce the principle that unrepaired strabismus promotes abnormal competition in V1, observable as interocular suppression of ODCs.     

Monocular and binocular optokinetic nystagmus in humans with defective stereopsis

In order to investigate the previously suggested relation between cortical binocular function and deficits in monocular optokinetic nystagmus (OKN), monocular and binocular OKN was examined in normal, stereodeficient, and stereoblind observers, using a variety of stimulation velocities and stimulus field sizes. Most stereodeficient and stereoblind observers showed monocular OKN deficits in one or both eyes, which took the form of either a directional asymmetry or a reduction of the response in both directions. The deficits were often more pronounced at higher stimulation velocities and with smaller stimulus field sizes. The severity of the OKN deficit was related to the degree of residual foveal stereopsis, while the type of the deficit seemed to be influenced by the presence and depth of amblyopia. Binocular OKN resembled the best monocular response in subjects with a directional or ocular asymmetry. The results fit well with current animal models of the neural control of OKN.     

The relevance of stereopsis for motorists: a pilot study

PURPOSE: To study the influence of stereoscopic depth perception on automobile driving performance. METHODS: Ten patients with strabismus and defective stereopsis were compared with ten healthy controls with respect to their performance in a series of automobile driving manoeuvres. The two groups were individually matched as to age, annual miles driven, years of licence holding and type of vehicle owned. After an ophthalmologic examination the subjects in each group performed the following series of driving tests: (1) stopping in front of an obstacle, (2) reversing into a parking space, (3) driving through a slalom course, (4) estimating the relative positions of two cars. All tests were performed binocularly and monocularly (with the non-dominant eye covered). RESULTS: Only in the slalom test did the normal subjects perform significantly better than the stereo-deficient subjects (odds ratio 10.5; P<0.01). In estimating position, normal subjects actually performed significantly worse (odds ratio 0.091; P<0.01). A significant distance ratio of 2.5 (95% CI 1.1-5.5; P=0.033) of the monocular with respect to the binocular performance of the normal subjects was found for the stopping task only, while the subjects with defective stereopsis showed no difference between their monocular and binocular performance. CONCLUSION: In this study, stereopsis had a positive effect on driving performance only in dynamic situations at intermediate distances.     

Influence of stereopsis and abnormal binocular vision on ocular and systemic discomfort while watching 3D television

Purpose

To evaluate the degree of three-dimensional (3D) perception and ocular and systemic discomfort in patients with abnormal binocular vision (ABV), and their relationship to stereoacuity while watching a 3D television (TV).

Methods

Patients with strabismus, amblyopia, or anisometropia older than 9 years were recruited for the ABV group (98 subjects). Normal volunteers were enrolled in the control group (32 subjects). Best-corrected visual acuity, refractive errors, angle of strabismus, and stereoacuity were measured. After watching 3D TV for 20 min, a survey was conducted to evaluate the degree of 3D perception, and ocular and systemic discomfort while watching 3D TV.

Results

One hundred and thirty subjects were enrolled in this study. The ABV group included 49 patients with strabismus, 22 with amblyopia, and 27 with anisometropia. The ABV group showed worse stereoacuity at near and distant fixation (P<0.001). Ocular and systemic discomfort was, however, not different between the two groups. Fifty-three subjects in the ABV group and all subjects in the control group showed good stereopsis (60 s of arc or better at near), and they reported more dizziness, headache, eye fatigue, and pain (P<0.05) than the other 45 subjects with decreased stereopsis. The subjects with good stereopsis in the ABV group felt more eye fatigue than those in the control group (P=0.031). The subjects with decreased stereopsis showed more difficulty with 3D perception (P<0.001).

Conclusions

The subjects with abnormal stereopsis showed decreased 3D perception while watching 3D TV. However, ocular and systemic discomfort was more closely related to better stereopsis.     

Monocular contribution to the peak time of the binocular pattern visual evoked potential

The contribution of each monocular pathway to the timing of the binocular pattern visual evoked potential was assessed in situations where a significant interocular timing discrepancy was observed. Monocular and binocular pattern visual evoked potentials to 0.5° checks were recorded from normal subjects, normal subjects in whom one eye was blurred, patients with monocular amblyopia, and patients with resolved unilateral optic neuritis. Normal subjects showed facilitation, while suppression was evidenced in subjects with monocular blurring. In patients with amblyopia, the affected pathway had no effect on binocular pattern visual evoked potential latency, suggesting that the amblyopic eye was suppressed. In contrast, all patients with optic neuritis showed binocular averaging. Our results show that different forms of binocular interaction are evidenced in normal subjects, in amblyopia and in optic neuritis, and suggest that a comparative analysis of monocular and binocular pattern visual evoked potential peak times brings valuable information to the clinical evaluation that could be used to distinguish disease processes further.Abbreviation BPVEP binocular pattern visual evoked potential