ANALYSIS OF A NATURALLY-OCCURRING ASYMMETRY IN VERTICAL SMOOTH PURSUIT EYE-MOVEMENTS IN A MONKEY

1. We have investigated the mechanism of a directional deficit in vertical pursuit eye movements in a monkey that was unable to match upward eye speed to target speed but that had pursuit within the normal range for downward or horizontal target motion. Except for a difference in the axis of deficient pursuit, the symptoms in this monkey were similar to those seen with lesions in the frontal or parietal lobes of the cerebral cortex in humans or monkeys. Our evaluation of vertical pursuit in this monkey suggests a new interpretation for the role of the frontal and parietal lobes in pursuit. 2. The up/down asymmetry was most pronounced for target motion at speeds greater-than-or-equal-to 2-degrees /s. For target motion at 15 or 30-degrees /s, upward step-ramp target motion evoked a brief upward smooth eye acceleration, followed by tracking that consisted largely of saccades. Downward step-ramp target motion evoked a prolonged smooth eye acceleration, followed by smooth, accurate tracking. 3. Varying the amplitude of the target step revealed that the deficit was similar for targets moving across all locations of the visual field. Eye acceleration in the interval 0-20 ms after the onset of pursuit was independent of initial target position and was symmetrical for upward and downward target motion. Eye acceleration in the interval 60-80 ms after the onset of pursuit showed a large asymmetry. For upward target motion, eye acceleration in this interval was small and did not depend on initial target position. For downward target motion, eye acceleration depended strongly on initial target position and was large when the target started close to the position of fixation. 4. We next attempted to understand the mechanism of the up/down asymmetry by evaluating the monkey's vertical motion processing and vertical eye movements under a variety of tracking conditions. For spot targets, the response to upward image motion was similar to that in normal monkeys if the image motion was presented during downward pursuit. In addition, the monkey with deficient upward pursuit was able to use upward image motion to make accurate saccades to moving targets. We conclude that the visual processing of upward image motion was normal in this monkey and that an asymmetry in visual motion processing could not account for the deficit in his upward pursuit. 5. Upward smooth eye acceleration was normal when the spot target was moved together with a large textured pattern. Upward and downward eye acceleration were nearly symmetrical, and the monkey was able to maintain upward eye speed that nearly matched target speed. We conclude that the up/down asymmetry in pursuit cannot be attributed to a deficit in the motor pathways that generate upward smooth eye movement. 6. In normal monkeys, pursuit velocity memory automatically sustains eye velocity, which therefore decelerates only slowly toward zero when the target is stabilized with respect to the moving eye. In the monkey with the up/down asymmetry, target stabilization caused eye velocity to decay faster during upward than during downward pursuit. However, the rate of decay during upward pursuit was similar to that in one of the control monkeys with normal vertical pursuit. We conclude that the up/down asymmetry cannot be attributed to a deficit in the mechanism of pursuit velocity memory. 7. Our observations suggest a model of pursuit that includes a switch in the visuomotor pathways for pursuit. If the monkey were able to close the switch for downward but not for upward target motion, then this kind of model would account for deficient upward pursuit with normal processing of upward image motion. A similar explanation could account for the directional deficits in horizontal pursuit seen after lesions of the parietal or frontal cortex, suggesting that these areas may play a larger role in the decision to pursue than in the direct visual guidance of pursuit.