Evidence for object permanence in the smooth-pursuit eye movements of monkeys

Abstract

We recorded the smooth-pursuit eye movements of monkeys in response to targets that were extinguished (blinked) for 200 ms in mid-trajectory. Eye velocity declined considerably during the target blinks, even when the blinks were completely predictable in time and space. Eye velocity declined whether blinks were presented during steady-state pursuit of a constant-velocity target, during initiation of pursuit before target velocity was reached, or during eye accelerations induced by a change in target velocity. When a physical occluder covered the trajectory of the target during blinks, creating the impression that the target moved behind it, the decline in eye velocity was reduced or abolished. If the target was occluded once the eye had reached target velocity, pursuit was only slightly poorer than normal, uninterrupted pursuit. In contrast, if the target was occluded during the initiation of pursuit, while the eye was accelerating toward target velocity, pursuit during occlusion was very different from normal pursuit. Eye velocity remained relatively stable during target occlusion, showing much less acceleration than normal pursuit and much less of a decline than was produced by a target blink. Anticipatory or predictive eye acceleration was typically observed just prior to the reappearance of the target. Computer simulations show that these results are best understood by assuming that a mechanism of eye-velocity memory remains engaged during target occlusion but is disengaged during target blinks.

FIG. 1

Schematic diagram illustrating the positions of the occluders and the target trajectories on the visual display. The trajectories used to examine pursuit initiation were presented on the top half of the display. The target moved at 35°/s and encountered an occluder (a) or underwent a blink (b) shortly after it began to move (the “occluded-initiation” and “blinked-initiation” conditions). The trajectories used to examine pursuit maintenance were presented on the bottom half of the display. The target moved at 15°/s and encountered an occluder (e) or underwent a blink (d) well after it began to move (the occluded-maintenance and blinked-maintenance conditions). Uninterrupted target trajectories, at both 15 and 35°/s (the “normal-maintenance” and “normal-initiation” conditions), were presented at position (c). The occluder is larger for the top trajectories because the target was moving faster, and we wished the occlusion/blink to last a constant duration.

FIG. 2

A representative response to the blinked-maintenance condition in which a target blink occurred after accurate pursuit was underway at 15°/s. Thin black lines show eye position and velocity. The sharp vertical deflections in the eye velocity trace correspond to saccades and have been clipped for presentation. Thick gray lines show target position and velocity. The time of the target blink is indicated by the blank interval on the target traces.

FIG. 3

Average responses from all monkeys tested for the 3 maintenance conditions. Responses to the blinked- and occluded-maintenance conditions are shown, respectively, by the solid and short dashed traces. For these 2 conditions, the closely overlapping thick gray lines and thin black lines show, respectively, saccade-interpolated and -excluded averages of eye velocity. For time points where more than half the responses were excluded from the saccade-excluded average, the trace is left blank. Averages are of 27–133 responses. SEs were, for most traces, little larger than the width of the traces and are not shown. The black bar at the bottom of each panel shows the duration of target absence. Responses to the normal-maintenance condition are shown by the thin, long-dashed trace. For this condition, saccade excluded and interpolated averages were essentially identical, and only the former is shown. A: responses of monkey P with each trace displaced vertically for optimal viewing. B–F: responses of monkeys P, Q, M, O, and N. The responses of monkey P in A and B are from 2 different days of testing. Monkey N was not shown the normal-maintenance condition. The thin vertical lines mark times that are 65 ms after the onset of the moving target, the disappearance of the target, and the reappearance of the target.

FIG. 4

Quantitative summary of the changes in eye velocity induced by target blinks and occlusion during pursuit maintenance. □, , and ▪, measurements made from the blinked-, normal-, and occluded-maintenance conditions. Decreases in eye velocity are graphed downward. The letter at the top of each set of bars indicates the monkey for whom the measures were made. Monkey P performed the experiment twice, yielding the measurements labeled “P1” and “P2.” The change in eye velocity for the blinked- and occluded-maintenance conditions was computed as the difference between eye velocity 80 ms after the disappearance of the target and the minimum eye velocity in the subsequent 300 ms. The change in eye velocity for the normal-maintenance condition was computed over the same interval as that for the blinked-maintenance condition (as there was typically no clear “minimum”). The error bars show SE, computed from the individual SEs of the 2 means. Monkey N was the 1st monkey tested and was not shown the normal-maintenance condition.

FIG. 5

A representative response during the blinked-initiation condition, in which the target was blinked shortly after the onset of target motion. Black traces show eye position and velocity. The sharp vertical deflection in the eye velocity trace corresponds to a saccade, and has been clipped for presentation. Thick gray traces show target position and velocity. The time of the target blink is indicated by the blank intervals in the target traces.

FIG. 6

Average eye velocity responses for conditions in which the target was blinked or occluded during the initiation phase of pursuit (A–C) or during the accelerating pursuit response to a change in target velocity (D). Saccade-interpolated and -excluded averages are shown, respectively, by the closely overlapping gray and black traces. The latter trace was left blank for time points where more than half the responses were excluded. Each panel contains three superimposed responses that correspond to the blinked (solid traces), occluded (short dashes), and normal (long dashes) conditions. A gray line shows the target velocity trajectory, with the gap indicating the time of target absence for the blinked and occluded conditions. A–C: responses during the initiation conditions for monkeys P, Q, and O. The thin vertical lines mark times that were 65 ms after the onset of the moving target, the disappearance of the target, and the reappearance of the target. D: responses during the velocity-change conditions for monkey M. For presentation, the full duration of pursuit at 5°/s is not shown. The thin vertical lines mark the same points as in C and D, except the 1st, which marks the time 65 ms after the target began to accelerate.

FIG. 7

Quantitative summary of the changes in eye velocity induced by target blinks and occlusion in the initiation, velocity-change, and delayed-initiation conditions. Increases in eye velocity are graphed upward, and decreases are graphed downward. Each triplet of bars shows data from 1 experiment. □, , and ▪, data from the blinked, normal, and occluded conditions, respectively. The letter at the top of each set of bars indicates the monkey for which the measures were made. When monkeys performed the experiment more than once (e.g., monkey P), this is indicated by the accompanying number. From left to right, the bars grouped along each x axis show data from 3 experimental paradigms: initiation, velocity-change, and delayed-initiation. The velocity-change conditions were presented in the same experimental sessions as the initiation conditions but were not presented to all monkeys. The delayed-initiation conditions were presented later in their own experimental sessions. Changes in eye velocity were computed as follows. First, the change in eye velocity was computed for the blinked condition as the difference between eye velocity 80 ms after the disappearance of the target (this time was always before the decline in eye velocity began) and the minimum eye velocity in the subsequent 300 ms. For the occluded and normal conditions, we then measured the change in eye velocity over the same interval, by making measurements from the same time points. Monkey O showed no dip in eye velocity during the blinked-initiation condition. We therefore measured the change in eye velocity from 80 ms after the disappearance of the target until 80 ms after the reappearance of the target (approximately the location of the minimum in eye velocity for the other monkeys). SEs were computed from the individual SEs of the 2 means. Measurements were made from the saccade-interpolated averages but were virtually identical if made from the saccade-excluded averages.

FIG. 8

Architecture and behavior of an image motion pursuit model. A: schematic diagram of the model. The arrows show the flow of signals and the elements in boxes represent various transformations. Ṫ, Ë, and Ý represent target, eye, and image velocity. After a delay (Δt), the image velocity input is processed by 2 pathways, the outputs of which are summed to create an eye acceleration command. The top pathway consists of a linear gain element and a filter and contributes a command that is proportional to image velocity. The bottom pathway consists of a nonlinear gain element, a differentiator, and a filter, and contributes a command that is related to image acceleration. Ë′is the net internal eye acceleration command and g₁ is a gain that operates as a switch; it is set to 1 only when the target is visible. Thus no visuo-motor command for eye acceleration is produced by the model during blinks or occlusion. The feedback loop that includes g₂ acts as an integrator to produce an eye velocity command, Ë′. When g₂ is 1, the integration is perfect; the loop produces an “eye-velocity memory” that can maintain stable pursuit in the absence of image motion. When g₂ is <1, eye velocity tends to decay toward 0 with a time constant determined by the value of g₂ and the time step of the simulation. The simulated eye velocity output of the model is produced by passing the eye velocity command, Ë′, through a filter that represents the compensated dynamics of the plant. B: simulated eye velocity for the normal (long dashes)-, occluded (short dashes)-, and blinked (solid trace)-maintenance conditions. C: simulated eye velocity for the normal (long dashes)-, occluded (short dashes)-, and blinked (solid trace)-initiation conditions. For both B and C, the bar at bottom shows the 200-ms duration of target absence. The thin vertical lines mark times 65 ms after the initial onset of target motion, the disappearance of the tracking target, and the reappearance of the tracking target.