Behavioral evaluation of movement cancellation

Abstract

The countermanding saccade task has been used in many studies to investigate the neural mechanisms that underlie the decision to execute or restrain rapid eye movements. In this task, the presentation of a saccade target is sometimes followed by the appearance of a stop cue that indicates that the subject should cancel the planned movement. Performance has been modeled as a race between motor preparation and cancellation processes. The signal that reaches its activation threshold first determines whether a saccade is generated or cancelled. In these studies, an important parameter is the time required to process the stop cue, referred to as the stop signal reaction time (SSRT). The SSRT is estimated using statistical approaches, the validity of which has not been unequivocally established. A more direct measure of this parameter might be obtainable if a method was available to "unmask" the developing motor command. This can be accomplished by air-puff-evoked blinks, which inhibit pontine omnipause neurons that serve as an inhibitory gate for the saccadic system. In the present study, brief puffs of air were used to elicit blinks at various times while rhesus monkeys performed a countermanding saccade task. If the developing motor command has not yet been cancelled, this should trigger a saccade. When blinks occurred between approximately 50 and 200 ms after target onset, saccades were often evoked. Saccades were rarely evoked more than approximately 70 ms after stop cue onset; this value represents a behavioral evaluation of SSRT and was comparable to the estimates obtained using standard statistical approaches. When saccades occurred near the SSRT on blink trials, they were often hypometric. Furthermore, Monte Carlo simulations were performed to model the effects of blink time on the race model. Overall, the study supports the validity of the statistical methods currently in use.

FIG. 1

Schematic of the target step (A) and countermanding (B) trial types. Top: visual display is schematically illustrated. - - -, imaginary windows within which the monkey is required to maintain gaze. To the right of B, 2 potential outcomes are shown. For the noncancelled trial, →,erroneous saccade to the green target. Bottom: sequence of events is schematized as black bars plotted against time. Modified from Paré and Hanes (2003).

FIG. 2

Schematic of the race model showing the expected effects of blinks. The stop and go processes race toward their respective thresholds (dashed red and solid green lines, respectively). If the go process finishes first, the movement is generated (noncancelled trial). If the stop process finishes first, the saccade is successfully cancelled. An eye blink effectively lowers the threshold for saccade initiation by turning off the omnipause neurons (OPNs, right). In some cases, this allows the go process to “win” the race when it would otherwise have “lost.”

FIG. 3

Single-trial examples of countermanding trials with blinks. Each eye position trace corresponds to the eyelid position trace of the same color below. Stop signal delays (SSDs) are the same for all trials within a panel (left, 150 for monkey WL; right, 160 for monkey TY). The effect of the blink on saccade generation depends on its timing (see text). The bottom portion of each panel shows the time course of the countermanding trial. In this and subsequent figures, data from the 2 monkeys are shown in the 2 columns.

FIG. 4

Effect of blink time on saccade latency. A: saccade latency is plotted as a function of blink time across all SSDs for all noncancelled trials, i.e., a saccade was generated. For monkey TY, the air-puff timing in the countermanding task was constrained to not evoke blinks >200 ms before target onset. The relationship between blink time and saccade latency is similar for target step (blue squares) and noncancelled countermanding trials (magenta circles). The effect of blink on saccade latency can be parsed into four clusters (Gandhi and Bonadonna 2005). Cluster 1, blinks occur long before target onset and have no effect on saccade latency; cluster 2, blinks occur around target onset and increase saccade latency, most likely because the eyes are closed or closing when the visual target is presented; cluster 3 (points covered in the dotted ellipse), blinks evoked after the saccade target is processed reduces saccade latency by triggering the eye movement during the blink itself; cluster 4, the blink is evoked after the saccade reaction time. This cluster categorization is referenced by the text describing Monte Carlo simulations of the race model. B: histograms of blink time for cancelled trials, i.e., no saccade generated. Binwidth = 25 ms.

FIG. 5

The effective interval of blink times for triggering saccades. A: histograms of blink time relative to stop cue onset for trials with blink-triggered saccades (□) and cancelled (■) trials. Note that blinks can evoke saccades only up to a particular point in time after the appearance of the stop cue. Bin width = 10 ms. B: panels plot the probability of the blink triggering a saccade, given that no saccade had yet occurred at the time of the blink. Bin width = 20 ms.

FIG. 6

Inhibition functions. A: panels illustrate the relationship between blink time re target onset, SSD, and saccade latency re target onset. Dots indicate trials in which the animal successfully cancelled the movement; circles show trials with saccades. The color of the circles indicates the saccade reaction time. B: inhibition functions for countermanding trials without blinks (black curve with stars) and for countermanding trials with blinks for various ranges of blink times. SSRT parameters were estimated for the nonblink trials only (see text).

FIG. 7

Lower boundary condition of the inequality test. It constrains, the cumulative density function (cdf) of saccade latency of non-cancelled trials for each SSD to be bounded below by the cdf of saccade latency of target-step trials. Each color trace is a cdf for 1 SSD, in increments of 25 ms. The thick, dashed (solid) black trace is the cdf plot from target-step trials with (without) blinks. This criterion is met for performance in countermanding trials without blinks (A) but violated for countermanding trials with blinks (B).

FIG. 8

Saccade latency relative to the stop cue is plotted as a function of blink time relative to target onset. Filled squares show upper bound values derived from an extreme value distribution fit to data binned in 50-ms increments according to blink time. Changes in color represent changes in SSD, in increments of 25 ms. Horizontal lines show statistical estimates of SSRT (see text) derived from nonblink trials: red, median method; dashed cyan, mean method; yellow line and shaded area, means ± SD of integration method.

FIG. 9

Saccade latency plotted as a function of stop cue onset for all blink times. Gray squares and circles are individual data points for countermanding trials with and without blinks, respectively. Red and blue filled squares indicate the medians of trials with and without blinks, respectively. Red and blue filled circles denote the upper bound of trials with and without blinks, respectively. For each SSD, the data have been offset slightly in x axis to facilitate visual comparison. Blue stars denote the SSDs for which the medians were significantly different (Wilcoxon test, P < 0.05). Insets: upper bound values for the two conditions are plotted against each other.

FIG. 10

Hypometria. Saccade amplitude (A) and probability (B) of observing a hypometric saccade, given that a saccade was generated, are plotted against saccade latency relative to stop cue onset. Data are from countermanding trials with (magenta circles) and without (blue squares) blinks. For both monkeys, hypometria was rare on trials without blinks, regardless of when the saccade occurred, but more prevalent after the onset of the stop cue in the blink trials.

FIG. 11

Saccade latency distributions for normometric (top) and hypometric (bottom) saccades show that the blinks induced dysmetria around the SSRT. Monkey WL: normometric saccades, −36 ± 74 (SD) ms; median, −22 ms. Extreme value distribution (EV) upper bound = 68 ms; EV mean = −3 ms. Hypometric saccades, 36 ± 69 ms; median = 61 ms. EV upper bound = 108 ms; EV mean = 61 ms. Medians of 2 distributions are significantly different (Wilcoxon test, P = 0). Median of hypometric distribution is also significantly different from upper bound of normometric saccades (signed-rank test, P = 8.2e-6). Monkey TY: normometric saccades, −6 ± 41 ms; median = −1 ms. EV upper bound = 59 ms; EV mean = 14 ms. Hypometric saccades: 31 ± 37 ms; median = 45 ms. EV upper bound = 83 ms; EV mean = 48 ms. Medians of 2 distributions are significantly different (Wilcoxon test, P = 0). Median of hypometric distribution is also significantly different from upper bound of normometric saccades (signed-rank test, P = 6.4e-10).

FIG. 12

Results of Monte Carlo simulations on trials without blinks. A: reciprobit plots (Carpenter 1981) illustrating both observed (—) and simulated (- - -) reaction time distributions are shown for the 2 animals. B: observed (—, ○) and simulated (- - -, □) inhibition functions are plotted in the 2 panels.

FIG. 13

Monte Carlo simulations of the motor preparation process during blinks. Distributions of observed saccade latency (blue squares) and simulated reaction times (red circles) are plotted as a function of blink time relative to target onset for target-step trials (A) and for noncancelled subset of countermanding trials (B). The blink-induced modification of the go process depends on the timing of the blink. See text for details.

FIG. 14

Results of Monte Carlo simulations on trials with blinks. Each panel plots 4 computed (“observed”) inhibition functions (dashed line, squares) from performance in countermanding trials. Each inhibition function, shown in a different color, was computed for a limited range of blink times, as indicated in the figure legend. These traces are the same as those plotted in Fig. 6B. The simulated inhibition function for each span of blink times is shown in the same color as circles connected by a solid line. This illustration shows that shifts in the inhibition functions can be simulated despite relatively similar stop rates across different blink times and suggests that blinks mainly modify the motor preparation process.