Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus

Observing a rotating visual pattern covering a large portion of the visual field induces optokinetic nystagmus (OKN). If the lights are suddenly switched off, optokinetic afternystagmus (OKAN) occurs. OKAN is hypothesized to originate in the velocity storage mechanism (VSM), a central processing network involved in multi-sensory integration. During a sustained visual rotation, the VSM builds up a velocity signal. After the lights are turned off, the VSM discharges slowly, with OKAN as the neurophysiological correlate. It has been reported that the initial afternystagmus in the direction of the preceding stimulus (OKAN-I) can be followed by a reversed one (OKAN-II), which increases with stimulus duration up to 15 min. In 11 healthy adults, we investigated OKAN following optokinetic stimulus lasting 30 s, 3-, 5-, and 10-min. Analysis of slow-phase cumulative eye position and velocity found OKAN-II in only 5/11 participants. Those participants presented it in over 70% of their trials with longer durations, but only in 10% of their 30 s trials. While this confirms that OKAN-II manifests predominantly after sustained stimuli, it suggests that its occurrence is subject-specific. We also did not observe further increases with stimulus duration. Conversely, OKAN-II onset occurred later as stimulus duration increased (p = 0.02), while OKAN-II occurrence and peak velocity did not differ between the three longest stimuli. Previous studies on OKAN-I, used negative saturation models to account for OKAN-II. As these approaches have no foundation in the OKAN-II literature, we evaluated if a simplified version of a rigorous model of OKAN adaptation could be used in humans. Slow-phase velocity following the trials with 3-, 5-, and 10-min stimuli was fitted with a sum of two decreasing exponential functions with opposite signs (one for OKAN-I and one for OKAN-II). The model assumes separate mechanisms for OKAN-I, representing VSM discharge, and OKAN-II, described as a slower adaptation phenomenon. Although the fit was qualitatively imperfect, this is not surprising given the limited reliability of OKAN in humans. The estimated adaptation time constant seems comparable to the one describing the reversal of the vestibulo-ocular reflex during sustained rotation, suggesting a possible shared adaptive mechanism.

Negative optokinetic afternystagmus in larval zebrafish demonstrates set-point adaptation

Motor learning is essential to maintain accurate behavioral responses. We used a larval zebrafish model to study ocular motor learning behaviors. During a sustained period of optokinetic stimulation in 5-day-old wild-type zebrafish larvae the slow-phase eye velocity decreased over time. Then interestingly, a long-lasting and robust negative optokinetic afternystagmus (OKAN) was evoked upon light extinction. The slow-phase velocity, the quick-phase frequency, and the decay time constant of the negative OKAN were dependent on the stimulus duration and the adaptation to the preceding optokinetic stimulation. Based on these results, we propose a sensory adaptation process during continued optokinetic stimulation, which, when the stimulus is removed, leads to a negative OKAN as the result of a changed retinal slip velocity set point, and thus, a sensorimotor memory. The pronounced negative OKAN in larval zebrafish not only provides a practical solution to the hitherto unsolved problems of observing negative OKAN, but also, and most importantly, can be readily applied as a powerful model for studying sensorimotor learning and memory in vertebrates.

The Main Sequence of Human Optokinetic Afternystagmus (OKAN)

Different types of fast eye movements, including saccades and fast phases of optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN), are coded by only partially overlapping neural networks. This is a likely cause for the differences that have been reported for the dynamic parameters of fast eye movements. The dependence of two of these parameters—peak velocity and duration—on saccadic amplitude has been termed “main sequence.” The main sequence of OKAN fast phases has not yet been analyzed. These eye movements are unique in that they are generated by purely subcortical control mechanisms and that they occur in complete darkness. In this study, we recorded fast phases of OKAN and OKN as well as visually guided and spontaneous saccades under identical background conditions because background characteristics have been reported to influence the main sequence of saccades. Our data clearly show that fast phases of OKAN and OKN differ with respect to their main sequence. OKAN fast phases were characterized by their lower peak velocities and longer durations compared with those of OKN fast phases. Furthermore we found that the main sequence of spontaneous saccades depends heavily on background characteristics, with saccades in darkness being slower and lasting longer. On the contrary, the main sequence of visually guided saccades depended on background characteristics only very slightly. This implies that the existence of a visual saccade target largely cancels out the effect of background luminance. Our data underline the critical role of environmental conditions (light vs. darkness), behavioral tasks (e.g., spontaneous vs. visually guided), and the underlying neural networks for the exact spatiotemporal characteristics of fast eye movements.

Expansion of Visual Space During Optokinetic Afternystagmus (OKAN)

The mechanisms underlying visual perceptual stability are usually investigated using voluntary eye movements. In such studies, errors in perceptual stability during saccades and pursuit are commonly interpreted as mismatches between actual eye position and eye-position signals in the brain. The generality of this interpretation could in principle be tested by investigating spatial localization during reflexive eye movements whose kinematics are very similar to those of voluntary eye movements. Accordingly, in this study, we determined mislocalization of flashed visual targets during optokinetic afternystagmus (OKAN). These eye movements are quite unique in that they occur in complete darkness and are generated by subcortical control mechanisms. We found that during horizontal OKAN slow phases, subjects mislocalize targets away from the fovea in the horizontal direction. This corresponds to a perceived expansion of visual space and is unlike mislocalization found for any other voluntary or reflexive eye movement. Around the OKAN fast phases, we found a bias in the direction of the fast phase prior to its onset and opposite to the fast-phase direction thereafter. Such a biphasic modulation has also been reported in the temporal vicinity of saccades and during optokinetic nystagmus (OKN). A direct comparison, however, showed that the modulation during OKAN was much larger and occurred earlier relative to fast-phase onset than during OKN. A simple mismatch between the current eye position and the eye-position signal in the brain is unlikely to explain such disparate results across similar eye movements. Instead, these data support the view that mislocalization arises from errors in eye-centered position information.