Vertical optokinetic nystagmus and vestibular nystagmus in the monkey: Up-down asymmetry and effects of gravity

Abstract

Vertical optokinetic nystagmus (OKN) i.e., OKN in the sagittal plane, was asymmetrical in the monkey when it was induced with animals lying on their sides in a 90° roll position. In typical monkeys the slow phase velocity of downward OKN (slow phases up) increased proportionally with stimulus velocity at close to unity gain to about 60°/s and saturated at about 100°/s. Upward OKN (slow phases down) increased with close to unity gain only to about 40°/s and saturated at about 60°/s. The slow phase velocity of upward OKN was usually irregular and its frequency was lower than that of downward or horizontal OKN. Upward and downward optokinetic afternystagmus (OKAN) were also asymmetrical. Upward OKAN was weak or absent and when present it usually saturated at 10°/s. Downward OKAN was stronger, increasing with a gain of about 0.7 with regard to stimulus velocity to a saturation velocity of about 50–60°/s. This was usually about 10–30°/s less than the saturation velocity of horizontal OKAN. The weak or absent upward OKAN indicates that stored activity related to slow phase eye velocity contributes little to the production of upward OKN. In agreement with this, there was little or no slow rise in slow phase velocity to a steady state level during upward OKN. Instead eye velocity rose to its peak velocity at the onset of stimulation. The lack of stored velocity information is probably largely responsible for the differences in regularity, gain and frequency between upward and downward OKN. Vertical vestibular nystagmus was induced by rotating monkeys in darkness with steps of velocity about a vertical axis, while they were lying on their sides in a 90° roll position. The velocities of the initial upward and downward slow phases were approximately equal. Gains of the vertical VOR ranged from about 0.5 to 0.98 for stimuli up to 1507s. Despite equivalent initial gains for upward and downward nystagmus, the vertical VOR was asymmetrical in that downward nystagmus had a higher frequency and generally lasted longer than upward nystagmus. Time constants of downward nystagmus (slow phases up) were about 15 s on average and were similar to those of horizontal nystagmus. Mean time constants of upward nystagmus (slow phases down) were about 8 s. This is only slightly longer than the average time constant of afferent activity in the semicircular canal nerves induced by steps of velocity. It indicates that stored activity related to slow phase velocity makes a smaller contribution to upward than downward or horizontal vestibular nystagmus. The asymmetry in vertical velocity storage was confirmed in experiments on visual-vestibular interactions. After rotation in light that evoked downward nystagmus, stored activity related to downward nystagmus cancelled or reduced upward post-rotatory nystagmus. Downward post-rotatory nystagmus was not diminished after rotation in light that had induced upward nystagmus. The difference between post-rotatory nystagmus after rotation in light and in darkness was approximately equal to the optokinetic after-nystagmus (OKAN) elicited by that velocity of rotation. Downward optokinetic or vestibular nystagmus was not suppressed as well as upward nystagmus when monkeys were exposed to a subject-stationary, visual surround. The eyes did not move into the slow phase direction during suppression of downward nystagmus, and slow phase eye velocity fell more slowly. In addition, stored activity was discharged more slowly during downward than horizontal nystagmus. Head position with respect to gravity had a striking effect on downward OKAN. When monkeys were upright, time constants of downward OKAN were much shorter and OKAN saturated at a lower velocity than when animals were in the lateral position. Consistent with reduced velocity storage in the upright position, downward OKN was irregular and had a lower saturation velocity than when animals were on their sides. When upward OKAN was present, it too was much weaker in the upright position. This indicates that information coming from the otolith organs plays an important role in conditioning the velocity storage mechanism responsible for vertical OKAN. The data show that there is an asymmetry in velocity storage for optokinetic and vestibular nystagmus in the sagittal plane when animals are out of the upright position. The presence of stored velocity information would enhance the low frequency characteristics of upward compensatory eye movements induced by the VOR during downward head movements. The functional significance of the asymmetry in the velocity storage mechanism for eye movements in the sagittal plane when animals are in the lateral or 90° roll position is not clear. However, these results parallel findings from experiments on movement perception in the sagittal plane of humans with subjects upright or on their sides (Young et al. 1975).