The influence of stimulus and behavioral histories on predictive control of smooth pursuit eye movements

The pursuit system has the ability to perform predictive control of eye movements. Even when the target motion is unpredictable due to velocity or direction changes, preceding changes in eye velocity are generated based on weighted averaging of past stimulus timing. However, it is still uncertain whether behavioral history influences the control of predictive pursuit. Thus, we attempted to clarify the influences of stimulus and behavioral histories on predictive pursuit to randomized target velocity. We used alternating-ramp stimuli, where the rightward velocity was fixed while the leftward velocity was either fixed (predictable) or randomized (unpredictable). Predictive eye deceleration was observed regardless of whether the target velocity was predictable or not. In particular, the predictable condition showed that the predictive pursuit responses corresponded to future target velocity. The linear mixed-effects model showed that both stimulus and behavioral histories of the previous two or three trials had influences on the predictive pursuit responses to the unpredictable target velocity. Our results suggest that the predictive pursuit system allows to track randomized target motion using the information from previous several trials, and the information of sensory input (stimulus) and motor output (behavior) in the past time sequences have partially different influences on predictive pursuit.

Mechanisms that allow cortical preparatory activity without inappropriate movement

We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in FEFSEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal allows for preparation to progress in the pursuit system without causing movement. We also show that preparatory modulation of firing rate in FEFSEM progresses in a way that predicts movement, providing evidence against the “movement-null” space hypothesis of how preparatory activity can progress without movement. Finally, there is partial reorganization of FEFSEM population activity between preparation and movement. We propose that this reorganization allows for a directionally non-specific component of preparatory visual-motor gain enhancement in the pursuit system.

The saccadic system does not compensate for the immaturity of the smooth pursuit system during visual tracking in children

Motor skills improve with age from childhood into adulthood, and this improvement is reflected in the performance of smooth pursuit eye movements. In contrast, the saccadic system becomes mature earlier than the smooth pursuit system. Therefore, the present study investigates whether the early mature saccadic system compensates for the lower pursuit performance during childhood. To answer this question, horizontal eye movements were recorded in 58 children (ages 5–16 yr) and 16 adults (ages 23–36 yr) in a task that required the combination of smooth pursuit and saccadic eye movements. Smooth pursuit performance improved with age. However, children had larger average position error during target tracking compared with adults, but they did not execute more saccades to compensate for their low pursuit performance despite the early maturity of their saccadic system. This absence of error correction suggests that children have a lower sensitivity to visual errors compared with adults. This reduced sensitivity might stem from poor internal models and longer processing time in young children.

Normal Pursuit-System Limitations— First Discovered in Infantile Nystagmus Syndrome

Infantile nystagmus syndrome (INS) patients occasionally have impaired pursuit. Model and patient data identified relative timing between target motion initiation and INS-waveform saccades as the cause. We used a new stimulus, the “step-pause-ramp” (SPR), to induce saccades proximal to target-velocity onset and test their effect on normal pursuit. Our OMS model predicted that proximal saccades impaired normal ramp responses, as in INS. Eye movements of subjects were calibrated monocularly and recorded binocularly; data were analyzed using OMtools software. Proximal saccades caused lengthened target acquisition times and steady-state position errors, confirming the model’s predictions. Spontaneous pursuit oscillation supported the hypothesis that INS is caused by loss of smooth-pursuit damping. Snooth pursuit may be impaired by saccades overlapping targetmotion onset.

A Unifying Model-Based Hypothesis for the Diverse Waveforms of Infantile Nystagmus Syndrome

We expanded the original behavioral Ocular Motor System (OMS) model for Infantile Nystagmus Syndrome (INS) by incorporating common types of jerk waveforms within a unifying mechanism. Alexander’s law relationships were used to produce desired INS null positions and sharpness. At various gaze angles, these relationships influenced the IN slow-phase amplitudes differently, thereby mimicking the gaze-angle effects of INS patients. Transitions from pseudopendular with foveating saccades to jerk waveforms required replacing braking saccades with foveating fast phases and adding a resettable neural integrator in the pursuit pre-motor circuitry. The robust simulations of accurate OMS behavior in the presence of diverse INS waveforms demonstrate that they can all be generated by a loss of pursuit-system damping, supporting this hypothetical origin.