The Vertical Vestibulo-Ocular Reflex, and Visual-Vestibular Interaction during Active Head Motion

533

Ann. N.Y. Acad. Sci. 956: 533–536 (2002). © 2002 New York Academy of Sciences.

The Vertical Vestibulo-Ocular Reflex, and Visual-Vestibular Interaction during Active Head Motion

JI SOO KIMa,b AND JAMES A. SHARPEa

aDivision of Neurology, University Health Network, University of Toronto, CanadabDepartment of Neurology, College of Medicine, Cheju National University, Cheju, Korea

KEYWORDS: vertical vestibulo-ocular reflex; visual-vestibular interaction;head motion

INTRODUCTION

The dynamics of vertical eye motion are reported to differ from those of horizon-tal motion.1,2 The characteristics of vestibular smooth eye motion during passivewhole-body rotation may differ from those during active head rotation.3 The verticalvestibulo-ocular reflex (VOR), its interactions with vision during active head mo-tion, and effects of aging on them had not been investigated.

METHODS

We measured smooth pursuit, combined eye-head tracking, the VOR, and its vi-sual enhancement and cancellation during active head motion in pitch using a mag-netic search coil technique in 21 younger (age < 65; mean, 36.4 ± 13.7) and 10elderly (age 65; mean, 77.6 ± 7.2) subjects. With the head immobile, subjects pur-sued a target moving sinusoidally with a frequency range of 0.125 to 2.0 Hz, andwith peak target accelerations (PTAs) ranging from 12 to 789°/sec2. Combined eye-head tracking, the VOR in darkness, and its visual enhancement during fixation ofan earth-fixed target (VVOR) were measured during active sinusoidal head rotationwith a peak-to-peak amplitude of 20° at frequencies of 0.25, 0.5, 1.0 and 2.0 Hz. Theefficacy of VOR cancellation was determined from VOR gains during combinedeye-head tracking.

Address for correspondence: James A. Sharpe, M.D., Division of Neurology, UniversityHealth Network, 399 Bathurst St., ECW 5-042, TWH, Toronto, ON, M5T 2S8, Canada. Voice:1-416-603-5950; fax: 1-416-603-5596.

sharpej@uhnres.utoronto.ca

534 ANNALS NEW YORK ACADEMY OF SCIENCES

RESULTS

Vertical smooth pursuit. Gains of upward and downward smooth pursuit de-clined with increasing frequency (p < 0.0001, ANOVA) (FIG. 1A). Both upward anddownward smooth pursuit gains decreased significantly with advancing age (Pear-son correlation coefficient, −0.80 < r < −0.63, p < 0.05).

Vertical eye-head tracking. Gaze gain decreased significantly as target fre-quency increased from 0.25 to 2.0 Hz (p < 0.0001, ANOVA) (FIG. 1B). Both up-ward and downward gaze (head plus eye motion) gains decreased with advancingage at frequencies from 0.25 to 1. 0Hz (Pearson correlation coefficient, −0.48 < r <−0.75, p < 0.005).

Vertical vestibulo-ocular reflex in darkness (VOR). The VOR gain or phasedid not vary with increasing age (Pearson correlation coefficient, −0.12 < r < 0.19,p > 0.5), except for downward movement at 0.25 Hz (FIG. 2A) where it decreasedin the elderly (p <0.05). Group mean gains did not vary with frequency or with headvelocity. Vestibular smooth eye movements were approximately 180° out of phasewith head movements.

FIGURE 1. (A) Smooth pursuit gains are plotted for a peak-to-peak target amplitudeof 20°. (B) Combined eye-head tracking. Gaze (eye plus head) gain declined with increasingfrequency in both age groups (p < 0.0001, repeated measures of ANOVA). Gains are great-er in the young than in the elderly. Error bars indicate 1 standard deviation.

535KIM & SHARPE: VOR DURING HEAD MOTION

Visual enhancement of the VOR (VVOR). No change in VVOR gain occurredwith advancing age (Pearson correlation coefficient, −0.40 < r < 0.32, p > 0.5). Fewelderly subjects could sustain tracking at 2.0 Hz, and in the younger group VVORgain decreased significantly at 2. 0Hz.

Visual cancellation of the VOR. VOR cancellation declined as target frequencyincreased (p <0.001, ANOVA). During combined eye-head tracking, cancellation ofthe vertical VOR deteriorated with advancing age at lower frequencies (0.25 and0.5 Hz) (Pearson correlation coefficient, −0.80 < r < 0.65, p 0.001).

DISCUSSION AND CONCLUSIONS

Quantitative investigation of vertical smooth pursuit, head-free tracking, theVOR in darkness, and visual enhancement of the VOR (VVOR) during active headmotion showed that vertical smooth pursuit, combined eye-head pursuit, and VORcancellation have common features of lowered gains at high target accelerations andsenescent degradation. The angular vertical VOR and VVOR vary little with advanc-ing age. VOR and VVOR performance in the elderly implicates relative preservationof neural structures subserving vertical vestibular smooth eye motion in senescence.

FIGURE 2. (A) Vestibulo-ocular reflex (VOR) gain. (B) Visual enhancement of VOR(VVOR). VOR and VVOR gains did not differ between younger and elderly groups and didnot vary with frequency. Error bars indicate 1 standard deviation.

536 ANNALS NEW YORK ACADEMY OF SCIENCES

ACKNOWLEDGMENTS

This work was supported by an Elizabeth Barford Award, University of Toronto(JSK), and by Canadian Institutes of Health Research (CIHR) Grants ME 5509 andMT 15362 (JAS).

REFERENCES

1. ROTTACH, K.G. et al. 1996. Comparison of horizontal, vertical and diagonal smoothpursuit eye movements in normal human subjects. Vision Res. 36: 2189–2195.

2. BALOH, R.W. et al. 1983. The dynamics of vertical eye movements in normal humansubjects. Aviat. Space Environ. Med. 54: 32–38.

3. DEMER, J.L., J.G. OAS & R.W. BALOH. 1993. Visual-vestibular interaction in humansduring active and passive, vertical head movement. J. Vestibular Res. 3:101–114.