Box plot conventions are similar to Figure 1. Perfectly conjugate saccades would have a ratio of 1. Upward saccades made by the patients are generally more conjugate than downward saccades. We found that the SD of gaze position was much larger in our two binocularly blind patients than in CS or in those with monocular visual loss Figure 3. Median eye speed was greatest in P7, who had been blind since birth Figure 4 ; she showed a wandering null point Figure 9A. P8, who had lost most binocular vision three years previously, showed eye drifts with speeds similar to that of monocularly affected patients Figure 9B.
A Gaze instability shown by P7, who had been blind since birth. Conventions are similar to Figure 2.
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B Gaze instability shown by P8, who had lost vision binocularly 3 years previously due to methanol poisoning. Horizontal gaze is disrupted by bidirectional drifts and saccadic intrusions; vertical gaze is disrupted by downbeat nystagmus. Finally, we asked how accurate eye movements could be in the case of P8, who had lost almost all of his vision 3 years previously.
He retained some visual perceptions of space and could walk from his house to his garage. Using his thumbs as a somatosensory cue, he was able to make quite accurate saccades Figure In contrast, P7, who had been blind since birth, was unable to make voluntary saccades, although her nystagmus showed frequent quick phases Figure 9A , implying that her brainstem saccade-generating mechanism was at least partly preserved. We set out to study the effects of monocular visual loss on binocular stability of gaze by making reliable eye movement recordings and comparing gaze stability in these patients with a group of healthy control subjects.
Prior studies have demonstrated that normal subjects can hold both eyes steady, even when one eye is occluded . We tested the hypothesis that the instability of gaze occurring with visual loss is a consequence mainly of loss of calibration of the neural network integrator for eye movements, which has been shown to contain component neurons that have monocular firing preference .
Two predictions of this hypothesis are that 1 loss of binocular visual cues, due to monocular impairment of vision, will affect gaze stability in both eyes, but mainly in the eye deprived of vision, and 2 eye movements dependent on projections to the ocular motoneurons that by-pass the neural integrator, such as the saccadic pulse command, will produce more conjugate movements than the eye drifts that occur during attempted fixation. Specifically, since individual burst neurons in the RIMLF project to motoneurons supplying elevator muscles of both eyes, due to axon collaterals  ,  , this circuitry would be expected to generate upward saccades that are consistently more conjugate than the eye drifts that occur during attempted fixation.
Our findings are generally supportive of this hypothesis. Vertical eye drifts occurring in eyes with visual loss were more disjunctive — by an order of magnitude — than vertical saccades. It is worthwhile noting that even normal subjects show some disconjugacy of vertical saccades when they shift gaze between two targets lying at different distances . An additional test of our hypothesis would be to compare the conjugacy of vertical eye movements in response to pitch head rotation and vertical optokinetic stimuli.
Our current study focused on head-fixed visual fixation and saccades, and we have only limited data from a prior study of vertical optokinetic responses that included Patient 1  and demonstrated no gain asymmetry. Thus, systematic measurements of the conjugacy of vertical vestibular and optokinetic response in subjects with monocular visual impairment seems justified. Our findings raise several issues for discussion.
First, why is gaze stability in the eye with impaired vision mainly in the vertical plane HBP?
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Second, why is gaze stability of the eye with better vision impaired compared with control subjects, especially when it is covered? Third, why does it take time for these instabilities to develop?
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Fourth, why does HBP with oscillopsia sometimes persist despite recovery to relatively normal vision? Vergence provides a robust, on-line mechanism to precisely align the eyes in the horizontal plane and, in Patient 1, was preserved, even though he lacked stereopsis. However, vertical vergence mechanisms show more limited range of movement and flexibility, although they are amenable to plastic-adaptive responses to changed visual demands, such as wearing a base-up prism before one eye . However, our patients were unable to use every-day disparity cues to improve gaze stability in their eye with impaired vision, even when visual acuity was near normal following restoration of vision P1 and P2.
The finding that gaze stability sometimes improved in the poorer eye when it was required to fix by covering the good eye was part of the original report of HBP . But why should gaze stability of the eye with better vision decrease when it was covered while the poor eye was viewing Figure 6? Similar behavior has been previously reported in amblyopic individuals . It is well established that most premotor signals for eye movements such as saccades are velocity coded, but that the final eye movement command must specify eye position, or else the eye would drift back to its center position due to elastic restoring forces in the orbit.
As noted in the Introduction , this neural integrator depends upon a distributed network of brainstem nuclei and the cerebellum. Although conventionally conceived as a network that guarantees conjugate gaze position, recent studies have emphasized the importance of constituent units with monocular preference .
If the neural integrator does guarantee the position of each eye, it needs to receive visual information from each eye to tune the balance of neurons such that the eyes move together. We propose that when lacking such inputs, the calibration of monocular units in the neural integrator deteriorates, leading to HBP. Bilateral loss of vision causes an even more severe breakdown in conjugate gaze holding, with continuous drifts of the eyes in ever-changing directions.
This drifting null phenomenon Figure 9 has also been reported following experimental cerebellectomy, which severely impairs the neural integrator function . Interestingly, gabapentin has been reported to suppress the HBP  ; this drug also suppresses forms of acquired pendular nystagmus that have been attributed to abnormalities instability of the neural integrator .
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Third, our studies of bilaterally blind patients stress the importance of the duration and age-of-onset of visual loss. Finally, one might ask why the HBP persists despite relatively normal vision P1 and P2 and oscillopsia. Development of oscillopsia after restoration of vision in an eye with HBP has been described by other groups of researchers . It seems paradoxical that patients with HBP can perceive visual motion, but cannot use it to prevent the eye from drifting.
Future studies to evaluate binocular tests of motion vision, such as deriving visual structure from motion, might provide insights into HBP, which is probably under-diagnosed, and which remains somewhat mysterious over a century after its original description. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Center for Biotechnology Information , U.
PLoS One. Published online Feb Rosalyn M. Schneider , 1 Matthew J. Matthew J. John Leigh. Susana Martinez-Conde, Editor. Author information Article notes Copyright and License information Disclaimer. Competing Interests: The authors have declared that no competing interests exist. Received Dec 3; Accepted Jan Copyright notice.
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This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. This article has been cited by other articles in PMC. Abstract When normal subjects fix their eyes upon a stationary target, their gaze is not perfectly still, due to small movements that prevent visual fading.
Introduction Eye movements evolved to serve vision . Table 1 Demographic and Clinical Information. Open in a separate window.
Results Visual Fixation Stability in Healthy Control Subjects Our first question was whether our healthy CS showed relative gaze instability evident as a greater SD of position of the eye under cover during monocular viewing. Figure 1. Summary of the stability of gaze in 20 healthy control subjects as they fixed upon a small visual target with one eye while their other eye was covered.
http://badgecommunity.com/882-cell-number-tracking.php Figure 2. Representative records comparing binocular fixation behavior in P1 with monocular visual impairment versus a control subject. Figure 3. Summary of measurements of gaze stability, expressed as SD of eye position, for 20 control subjects box plots and for individual patients studied for each directional component. Figure 4. Summary of measurements of gaze stability, expressed as median eye speed, for 20 control subjects box plots and for individual patients studied for each directional component.
Figure 5. Representative records comparing the disconjugacy of gaze for each directional component for P1 with monocular visual impairment versus a control subject. Figure 6. Representative record from P1 comparing the effects of monocular viewing with either eye. Upward Saccades with Monocular Visual Loss To test the second part of our hypothesis — that eye movements due to signals passing directly to ocular motoneurons will be less affected by monocular loss of visual inputs — we measured the conjugacy of vertical saccades in P, and compared them with control subjects.
Figure 7. Representative record of vertical saccades made by P1. Figure 8.
Binocular Visual Loss We found that the SD of gaze position was much larger in our two binocularly blind patients than in CS or in those with monocular visual loss Figure 3. Figure 9. Representative records of gaze instability in two patients with bilateral visual loss. Figure The saccades are generally accurate and conjugate, despite upward drifts of gaze.
Discussion We set out to study the effects of monocular visual loss on binocular stability of gaze by making reliable eye movement recordings and comparing gaze stability in these patients with a group of healthy control subjects. Acknowledgments We are grateful to Dr. David Zee for helpful discussions. References 1. Walls GL The evolutionary history of eye movements. Vision Res 2 : 69— Oxford University Press: New York.
Nat Rev Neurosci 5 : — J Neurosci 32 : — Carpenter RHS The visual origins of ocular motility.