Neurological basis for eye movements of the blind

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. Visual loss is known to cause greater instability of gaze, but reported comparisons with normal subjects using reliable measurement techniques are few. We measured binocular gaze using the magnetic search coil technique during attempted fixation (monocular or binocular viewing) of 4 individuals with childhood-onset of monocular visual loss, 2 individuals with late-onset monocular visual loss due to age-related macular degeneration, 2 individuals with bilateral visual loss, and 20 healthy control subjects. We also measured saccades to visual or somatosensory cues. We tested the hypothesis that gaze instability following visual impairment is caused by loss of inputs that normally optimize the performance of the neural network (integrator), which ensures both monocular and conjugate gaze stability. During binocular viewing, patients with early-onset monocular loss of vision showed greater instability of vertical gaze in the eye with visual loss and, to a lesser extent, in the normal eye, compared with control subjects. These vertical eye drifts were much more disjunctive than upward saccades. In individuals with late monocular visual loss, gaze stability was more similar to control subjects. Bilateral visual loss caused eye drifts that were larger than following monocular visual loss or in control subjects. Accurate saccades could be made to somatosensory cues by an individual with acquired blindness, but voluntary saccades were absent in an individual with congenital blindness. We conclude that the neural gaze-stabilizing network, which contains neurons with both binocular and monocular discharge preferences, is under adaptive visual control. Whereas monocular visual loss causes disjunctive gaze instability, binocular blindness causes both disjunctive and conjugate gaze instability (drifts and nystagmus). Inputs that bypass this neural network, such as projections to motoneurons for upward saccades, remain conjugate.

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.

Panel A shows the distribution of measurements of standard deviation (SD) of eye position; the percentile values on these box plots, and in subsequent figures, are indicated (50% is the median). Panel B summarizes median speed of eye drifts during monocular fixation. For the group of subjects, there was no significant difference in the SD of eye position or median speed between the viewing and covered eyes.

Figure 2. Representative records comparing binocular fixation behavior in P1 with monocular visual impairment versus a control subject.

The scales are similar to allow direct comparison between P1 (A) and the control subject (B). In this and similar subsequent time plots of eye movements, positive values indicate eye rotations to the right, upward, or clockwise from the subject’s viewpoint. At the top, visual acuity of each eye is stated. At the right, the SD of eye position (in degrees) is specified for each directional component of their eye movements. REH: right eye horizontal; LEH left eye horizontal; REV: right eye vertical; LEV: left eye vertical; RET: right eye torsional; LET: left eye torsional. Note the increased instability of gaze in P1’s left eye, especially in the vertical plane (LEV). The asterisk indicates that the SD value is significantly larger (p<0.05) than pooled data from normal subjects.

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.

Note how especially vertical gaze has greater SD values, indicating greater instability, in the poor eye (lower visual acuity) of patients with monocular visual loss compared with control subjects. Also note how P7 and P8, with binocular visual loss, have much greater SD values (most unstable gaze) compared with either control subjects or patients with monocular visual loss. Outlier values are stated at the top of the plot.

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.

For patients with monocular visual loss, SD values of eye speed were greater in the eyes with poorer vision (less so for P5 and P6 with late onset of visual loss due to ARMD). The fastest eye-drift speeds were shown by P7, who had been blind since birth.

Figure 5. Representative records comparing the disconjugacy of gaze for each directional component for P1 with monocular visual impairment versus a control subject.

(A): Record of P1. (B): Record of control subject. Values shown at right of each plot are SD of the difference between right and left eye position for each directional component. One asterisk indicates that the SD value is significantly larger (p<0.05) than pooled data from normal subjects; two asterisks indicate p<0.01. See caption to Figure 2 for further details.

Figure 6. Representative record from P1 comparing the effects of monocular viewing with either eye.

A: Viewing with the eye with better visual acuity (see cartoon at bottom). B: Viewing with the eye with poorer visual acuity (see cartoon at top). During fixation with the good, right eye (A), drifts are evident in the covered left eye, especially vertically. When the bad eye attempts to fixate the small visual target (B), gaze becomes more stable for that eye, but the good eye under cover shows increased drifts.

Figure 7. Representative record of vertical saccades made by P1.

The left axis displays eye and target position and the right axis displays eye velocity. Target position is indicated by the dotted line. The first, downward saccade (S1) is mildly disjunctive (right eye, red trace, moves farther), although peak velocities of the two eyes are similar. Subsequently, the left eye (blue trace) drifts away from the target (D1). The second, upward saccade (S2), which has a small overshoot, starts with the eyes at different positions, but the change in eye position is similar and the velocity profiles are very conjugate (overlapping records).

Figure 8. Summary of measurements of ratio of peak velocity of bad eye/peak velocity of good eye for upward and downward saccades of the group of control subjects (CS) and P1-4, who had monocular loss of vision early in life.

Box plot conventions are similar to Figure 1. Perfectly conjugate saccades would have a ratio of 1.0. Upward saccades made by the patients are generally more conjugate than downward saccades.

Figure 9. Representative records of gaze instability in two patients with bilateral visual loss.

(A) Gaze instability shown by P7, who had been blind since birth. Conventions are similar to Figure 2. The records show continuous eye drifts and nystagmus that changes direction, implying a “wandering null” or variable set point of the gaze-holding mechanism. (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. Double asterisks indicate SD values significantly different (p<0.01) from control subjects.

Figure 10. Vertical saccades made by P8 to his (unseen) thumbs located at positions above and below his eye level, subtending a visual arc measured to be 38°.

The saccades are generally accurate and conjugate, despite upward drifts of gaze.