Time course of motor preparation during visual search with flexible stimulus-response association

Abstract

Whether allocation of visuospatial attention can be divorced from saccade preparation has been the subject of intense research efforts. A variant of the visual search paradigm, in which a feature singleton indicates that the correct saccade should be directed to it (prosaccade) or to the opposite distractor (antisaccade), has been influential in addressing this core topic. We performed a causal assessment of this controversy by delivering an air puff to one eye to invoke the trigeminal blink reflex as monkeys performed this visual search task. Blinks effectively remove saccadic inhibition and prematurely trigger impending saccades in reaction time tasks, thus providing a behavioral readout of the premotor plan. We found that saccades accompanied blinks during the initial allocation of attention epoch and that these movements were directed to the singleton for both prosaccade and antisaccade trials. Blinks evoked at later times were accompanied with saccades to the correct end point location: the singleton on prosaccade trials and the opposite distractor on antisaccade trials. These results provide support for concurrent encoding of visuospatial attention and saccade preparation during visual search behavior.

Figure 1.

Spatiotemporal illustrations of combined saccade–blink movements. A, Horizontal and vertical eye amplitude and velocities (top four rows) and eyelid amplitude (bottom row) are plotted as a function of time. Four representative eye movements are shown. The dashed black line indicates array onset. Red trace denotes an “early blink” trial, in which the blink occurs during the fixation interval. The actual saccade occurs at a regular latency after array onset. Magenta trace represents a trial in which the blink was timed too late; it occurred after the saccade. The green trace identifies a “blink-triggered” movement, in which the saccade accompanies the blink. Such saccades are prematurely triggered, as evidenced by the shorter latency. The black trace indicates a control saccade without a blink. Scale bars: horizontal and vertical eye positions, 5°; horizontal and vertical eye velocities, 200°/s; eyelid position, arbitrary units. B, The same movements are represented as spatial trajectories. All traces begin near the origin. The early-blink trial (red trace) shows that the blink-induced eye movement is a loopy perturbation with a small horizontal and a larger vertical component. The eyes return close to their original position well before the rightward eye movement is produced. The magenta trace shows a similar loopy movement after the horizontal saccade is completed. The blink-triggered trial (green trace) starts off as a loopy movement, then deviates from the trajectory in midflight and produces an oblique saccade that reaches the target location. A Euclidean algorithm, which identifies the position and instance the blink-triggered movement deviates from an early-blink template (arrow), was used to detect saccade onset.

Figure 2.

Predictions of blink perturbation on saccade generation for the PMTA and discrete processes hypotheses. A, Prosaccade (left) and antisaccade (right) trials were indicated by the color of a singleton among identical distractors in a visual search array. B, Schematized activity patterns in visually responsive “singleton neuron” (when the singleton is placed in its receptive field) and an “antineuron” (when the opposite distractor is placed in its receptive field). Green and red traces are schematics of activity patterns of singleton neuron and antineuron, respectively. Waveforms have been adapted from FEF data (compare Sato and Schall, 2003, their Fig. 2A, left column). The initial sensory response is similar in both neurons. For prosaccade trials (left), activity continues to accumulate in the singleton neuron and is suppressed in the antineuron. The vertical dashed line indicates the time when activities in the two neurons become significantly different. For antisaccade trials (right), the enhancement in activity of the singleton neuron is short lived (arrow). It begins to attenuate as activity in the antineuron becomes enhanced, indicating selection of the opposite distractor and, perhaps, the formulation of a new motor plan to produce an antisaccade. As in the prosaccade condition, the first vertical dashed line identifies the time when activities in the two neurons initially become significantly different (singleton neuron shows enhancement). The second vertical line marks the time when activity in the antineuron becomes higher. Epoch 1 refers to the period for which the green trace is greater than the red trace, while Epoch 2 spans the duration for which the red trace resides above the green trace. C, Predictions of saccade direction (toward singleton or antisaccade end point) as a function of latency of blink-triggered saccades. For the PMTA, a blink triggers a saccade if activities in the singleton neuron and antineuron are significantly different, and the saccade will be directed to the neuron with higher activity. Thus, on prosaccade trials, the blink is an effective trigger for all time points after the first vertical dashed line (Epoch 1, as in B), and all saccades should be directed to the singleton (solid green line). During antisaccade trials, blinks invoked during Epoch 1 (in between the two vertical dashed lines) should produce reduced latency saccades to the singleton (solid green line), while blinks evoked during Epoch 2 should direct saccades to the opposite distractor (solid purple line). For the discrete processes hypothesis, accumulation in motor neurons (data not shown) initiate after target selection is complete. For prosaccades, the effectiveness of the blink to trigger a saccade (dashed green line) will be delayed compared to the PMTA. For antisaccade trials, target selection of the singleton must be suppressed and the opposite distractor target must be selected before motor preparation commences. Thus, a blink evoked during Epoch 1 (in between the two vertical lines) should not trigger a saccade, which is denoted by the absence of a dashed green line in this epoch. Activity in motor neurons will initiate in Epoch 2, but only after target selection is complete. Only after this criterion is fulfilled will a blink become an effective perturbation for triggering a saccade (dashed purple line). Note that the shortest saccade latency is slightly delayed compared to the PMTA prediction. The differential effect predicted for antisaccade trials is the focus of the study. The vertical offset between the saccade direction predictions (horizontal solid and dashed lines) is only for illustration purposes.

Figure 3.

Blink effects on the latency of saccades executed during visual search (step task). A, C, The latency of saccades evoked during prosaccade trials as a function of the time of blink relative to saccade cue. Each dot represents a puff/blink trial. Every blue point represents a successful saccade to the singleton, red a failure to the antisaccade end point, and green a failure to one of the orthogonal distractors. B, D, The latency of saccades evoked during antisaccade trials as a function of the occurrence of blink relative to saccade cue. Each blue point represents a successful trial to the antisaccade end point (opposite distractor), red a failure to the singleton, and green a failure to one of the orthogonal distractors. In each panel, the data encircled in the ellipse represent blink-triggered movements (for criterion, see Materials and Methods). Each row illustrates data from one animal.

Figure 4.

Direction of blink-triggered movements executed during visual search (step task). A, C, The direction of blink-triggered saccades, those encompassed in the dotted ellipse in Figure 3, evoked during prosaccade trials as a function of saccade latency. Each blue point represents a successful trial to the singleton, red a failure to the antisaccade end point, and green a failure to one of the orthogonal distractors. B, D, The direction of blink-triggered saccades evoked during antisaccade trials as a function of saccade latency. Each blue point represents a successful trial to the antisaccade end point (opposite distractor), red a failure to the singleton, and green a failure to one of the orthogonal distractors. The cyan line illustrates a moving average across saccade latency. The eye position at the end of the primary saccade relative to the initial eye position (close to origin) was used to calculate the direction metric for each trial. Each row illustrates data from one animal.

Figure 5.

End points of blink-triggered saccades executed during visual search (step task). A, The distribution of end points of every blink-triggered movement from both animals is plotted for prosaccade trials. The location of the singleton was always rotated to (10°, 0°) so that all correct movements (blue) are to the right, failures to the opposite distractor (red) are to the left, and failures to the orthogonal distractors (green) are to up or down locations. B, The distribution of end points of every blink-triggered movement from both animals is plotted for antisaccade trials. The same location (10°, 0°) is used for the singleton. Thus, correct saccades to the opposite distractor (blue) are to the left, failures to the singleton (red) are to the right, and failures to an orthogonal distractor (green) are to up or down locations.

Figure 6.

Effects of blinks during visual search in the gap-task. A, B, Saccade latency is plotted as a function of occurrence of blink relative to saccade cue for prosaccade (A) and antisaccade (B) trials. Blink-triggered saccades are denoted by points within the dotted ellipses. C, D, The directions of these blink-triggered saccades are plotted as a function of saccade latency for prosaccade (C) and antisaccade (D) trials. For prosaccade data (left), each blue point represents a successful trial to the singleton, red a failure to the antisaccade end point, and green a failure to one of the orthogonal distractors. For antisaccade trials (right), each blue dot represents a successful trial to the antisaccade end point, red a failure to the singleton, and green a failure to one of the orthogonal distractors. The cyan line illustrates a moving average across saccade latency (bin size, 30 ms). The eye position at the end of the primary saccade relative to the initial eye position (close to origin) was used to calculate the direction metric for each trial. Data from only one monkey are shown. Data from second animal were similar.

Figure 7.

Effects of blinks during visual search in the delay task. Data collected from one animal performing the delayed saccade variant of the search task are shown in exactly the same format as in Figure 6. For prosaccade data (left), each blue point represents a successful trial to the singleton, red a failure to the antisaccade end point, and green a failure to one of the orthogonal distractors. For antisaccade trials (right), each blue dot represents a successful trial to the antisaccade end point, red a failure to the singleton, and green a failure to one of the orthogonal distractors. The cyan line illustrates a moving average across saccade latency. The eye position at the end of the primary saccade relative to the initial eye position (close to origin) was used to calculate the direction metric for each trial. Note the dearth of saccades to the singleton during antisaccade trials. Data from second animal were similar.