The smooth pursuit eye movement system uses retinal information about the image-slip-velocity of the target in order to match the eye-velocity-in-space (i.e., gaze-velocity) to the actual target velocity. To maintain the target image on the fovea during smooth gaze tracking, and to compensate for the long delays involved in processing visual motion information and/or eye velocity commands, the pursuit system must use prediction. We have shown recently that both retinal image-slip-velocity and gaze-velocity signals are coded in the discharge of single pursuit-related neurons in the simian periarcuate cortex. To understand how periarcuate pursuit neurons are involved in predictive smooth pursuit, we examined the discharge characteristics of these neurons in trained Japanese macaques. When a stationary target abruptly moved sinusoidally along the preferred direction at 0.5 Hz, the response delays of pursuit cells seen at the onset of target motion were compensated in succeeding cycles. The monkeys were also required to continue smooth pursuit of a sinusoidally moving target while it was blanked for about half of a cycle at 0.5 Hz. This blanking was applied before cell activity normally increased and before the target changed direction. Normalized mean gain of the cells' responses (re control value without blanking) decreased to 0.81(+/-0.67 SD), whereas normalized mean gain of the eye movement (eye gain) decreased to 0.65 (+/-0.16 SD). A majority (75%) of pursuit neurons discharged appropriately up to 500 ms after target blanking even though eye velocity decreased sharply, suggesting a dissociation of the activity of those pursuit neurons and eye velocity. To examine whether pursuit cell responses contain a predictive component that anticipates visual input, the monkeys were required to fixate a stationary target while a second test laser spot was moved sinusoidally. A majority (68%) of pursuit cells tested responded to the second target motion. When the second spot moved abruptly along the preferred direction, the response delays clearly seen at the onset of sinusoidal target motion were compensated in succeeding cycles. Blanking (400-600 ms) was also applied during sinusoidal motion at 1 Hz before the test spot changed its direction and before pursuit neurons normally increased their activity. Preferred directions were similar to those calculated for target motion (normalized mean gain=0.72). Similar responses were also evoked even if the second spot was flashed as it moved. Since the monkeys fixated the stationary spot well, such flashed stimuli should not induce significant retinal slip. These results taken together suggest that the prediction-related activity of periarcuate pursuit neurons contains extracted visual components that reflect direction and speed of the reconstructed target image, signals sufficient for estimating target motion. We suggest that many periarcuate pursuit neurons convey this information to generate appropriate smooth pursuit eye movements.

Through the development of a high-acuity fovea, primates with frontal eyes have acquired the ability to use binocular eye movements to track small objects moving in space. The smooth-pursuit system moves both eyes in the same direction to track movement in the frontal plane (frontal pursuit), whereas the vergence system moves left and right eyes in opposite directions to track targets moving towards or away from the observer (vergence tracking). In the cerebral cortex and brainstem, signals related to vergence eye movements--and the retinal disparity and blur signals that elicit them--are coded independently of signals related to frontal pursuit. Here we show that these types of signal are represented in a completely different way in the smooth-pursuit region of the frontal eye fields. Neurons of the frontal eye field modulate strongly during both frontal pursuit and vergence tracking, which results in three-dimensional cartesian representations of eye movements. We propose that the brain creates this distinctly different intermediate representation to allow these neurons to function as part of a system that enables primates to track and manipulate objects moving in three-dimensional space.

The smooth pursuit system interacts with the vestibular system to maintain the accuracy of eye movements in space. To understand neural mechanisms of short-term modifications of the vestibulo-ocular reflex (VOR) induced by pursuit-vestibular interactions, we used a cross-axis procedure in trained monkeys. We showed earlier that pursuit training in the plane orthogonal to the rotation plane induces adaptive cross-axis VOR in complete darkness. To further study the properties of adaptive responses, we examined here the initial eye movements during tracking of a target while being rotated with a trapezoidal waveform (peak velocity 30 or 40 degrees/s). Subjects were head-stabilized Japanese monkeys that were rewarded for accurate pursuit. Whole body rotation was applied either in the yaw or pitch plane while presenting a target moving in-phase with the chair with the same trajectory but in the orthogonal plane. Eye movements induced by equivalent chair rotation with or without the target were examined before and after training. Before training, chair rotation alone resulted only in the collinear VOR, and smooth eye movement-tracking of orthogonal target motion during rotation had a normal smooth pursuit latency (ca 100 ms). With training, the latency of orthogonal smooth tracking eye movements shortened, and the mean latency after 1 h of training was 42 ms with a mean gain, at 100 ms after stimulus onset, of 0.4. The cross-axis VOR induced by chair rotation in complete darkness had identical latencies with the orthogonal smooth tracking eye movements, but its gains were <0.2. After cross-axis pursuit training, target movement alone without chair rotation induced smooth pursuit eye movements with latencies ca 100 ms. Pursuit training alone for 1 h using the same trajectory but without chair rotation did not result in any clear change in pursuit latency (ca 100 ms) or initial eye velocity. When a new target velocity was presented during identical chair rotation after training, eye velocity was correspondingly modulated by just 80 ms after rotation onset, which was shorter than the expected latency of pursuit (ca 100 ms). These results indicate that adaptive changes were induced in the smooth pursuit system by pursuit-vestibular interaction training. We suggest that this training facilitates the response of pursuit-related neurons in the cortical smooth pursuit pathways to vestibular inputs in the orthogonal plane, thus enabling smooth eye movements to be executed with shorter latencies and larger eye velocities than in normal smooth pursuit driven only by visual feedback.

The smooth pursuit system moves the eyes in space accurately while compensating for visual inputs from the moving background and/or vestibular inputs during head movements. To understand the mechanisms underlying such interactions, we examined the influence of a stationary textured visual background on smooth pursuit tracking and compared the results in young and adult humans and monkeys. Six humans (three children, three adults) and six macaque monkeys (five young, one adult) were used. Human eye movements were recorded using infrared oculography and evoked by a sinusoidally moving target presented on a computer monitor. Scleral search coils were used for monkeys while they tracked a target presented on a tangent screen. The target moved in a sinusoidal or trapezoidal fashion with or without whole body rotation in the same plane. Two kinds of backgrounds, homogeneous and stationary textured, were used. Eye velocity gains (eye velocity/target velocity) were calculated in each condition to compare the influence of the textured background. Children showed asymmetric eye movements during vertical pursuit across the textured (but not the homogeneous) background; upward pursuit was severely impaired, and consisted mostly of catch-up saccades. In contrast, adults showed no asymmetry during pursuit across the different backgrounds. Monkeys behaved similarly; only slight effects were observed with the textured background in a mature monkey, whereas upward pursuit was severely impaired in young monkeys. In addition, VOR cancellation was severely impaired during upward eye and head movements, resulting in residual downward VOR in young monkeys. From these results, we conclude that the directional asymmetry observed in young primates may reflect a different neural organization of the vertical, particularly upward, pursuit system in the face of conflicting visual and vestibular inputs that can be associated with pursuit eye movements. Apparently, proper compensation matures later.

Shinmei, Yasuhiro, Takanobu Yamanobe, Junko Fukushima, and Kikuro Fukushima. Purkinje cells of the cerebellar dorsal vermis: simple-spike activity during pursuit and passive whole-body rotation. J Neurophysiol 87: 1836J Neurophysiol 87: -1849J Neurophysiol 87: , 2002 10.1152/jn.00150.2001. To track a slowly moving object during whole body rotation, smoothpursuit and vestibularly induced eye movements must interact to maintain the accuracy of eye movements in space (i.e., gaze), and gaze movement signals must eventually be converted into eye movement signals in the orbit. To understand the role played by the cerebellar vermis in pursuit-vestibular interactions, in particular whether the output of the vermis codes gaze-velocity or eye-velocity, we examined simple-spike activity of 58 Purkinje (P-) cells in lobules VI-VII of head-stabilized Japanese monkeys that were trained to elicit smooth-pursuit eye movements and cancel their vestibuloocular reflex (VOR) during passive whole body rotation around horizontal, vertical, or oblique axes. All pursuit-sensitive vermal P-cells also responded during VOR cancellation, and the majority of them had peak modulation near peak stimulus velocity. The directions of maximum modulation during these two tasks were distributed in all directions with a downward preponderance. Using standard criteria, 40% of pursuitsensitive vermal P-cells were classified as gaze-velocity. Other P-cells were classified either as eye/head-velocity group I (36%) that had similar preferred directions during pursuit and VOR cancellation but that had larger responses during VOR ϫ1 when gaze remained stationary, or as eye/head-velocity group II (24%) that had oppositely directed or orthogonal eye and head movement sensitivity during pursuit and VOR cancellation. Eye/head-velocity group I P-cells contained cells whose activity was correlated with eye velocity. Modulation of many P-cells of the three groups during VOR ϫ1 could be accounted for by the linear addition of their modulations during pursuit and VOR cancellation. When monkeys fixated a stationary target, over half of the P-cells tested, including gaze-velocity P-cells, discharged in proportion to the velocity of retinal motion of a second spot. These observations are in a striking contrast to our previous results for floccular vertical P-cells. Because we used identical tasks, these differences suggest that the two cerebellar regions are involved in very different kinds of processing of pursuit-vestibular interactions.