Controlled movement processing: superior colliculus activity associated with countermanded saccades

Abstract

We investigated whether the monkey superior colliculus (SC), an important midbrain structure for the regulation of saccadic eye movements, contains neurons with activity patterns sufficient to control both the cancellation and the production of saccades. We used a countermanding task to manipulate the probability that, after the presentation of a stop signal, the monkeys canceled a saccade that was planned in response to an eccentric visual stimulus. By modeling each animal's behavioral responses, with a race between GO and STOP processes leading up to either saccade initiation or cancellation, we estimated that saccade cancellation took on average 110 msec. Neurons recorded in the superior colliculus intermediate layers during this task exhibited the discharge properties expected from neurons closely involved in behavioral control. Both saccade- and fixation-related discharged differently when saccades were counter-manded instead of executed, and the time at which they changed their activity preceded the behavioral estimate of saccade cancellation obtained from the same trials by 10 and 13 msec, respectively. Furthermore, these intervals exceed the minimal amount of time needed for SC activity to influence eye movements. The additional observation that saccade-related neurons discharged significantly less when saccades were countermanded instead of executed suggests that saccades are triggered when these neurons reach a critical activation level. Altogether, these findings provide solid evidence that the superior colliculus contains the necessary neural signals to be directly involved in the decision process that regulates whether a saccade is to be produced.

Figure 1.

Trial displays for the countermanding saccade task. Each trial began with the fixation of a central fixation point (FP) for a variable interval after which it disappeared and a target (T) simultaneously appeared, either in the response field of the neuron or in the opposite hemifield. In the CONTROL trials, monkeys were rewarded for responding with a single targeting saccade (left). On a fraction of interleaved trials (right), the fixation point reappeared after a variable delay (SSD) and acted as a stop signal instructing the monkeys to withhold saccade initiation. In these STOP trials, they were rewarded for countermanding the planned movement and maintaining fixation on the fixation point (canceled STOP trials). No reward was delivered if they responded with a targeting saccade (noncanceled STOP trials). The dotted circle and arrow indicate current gaze position and saccade vector during each interval, respectively.

Figure 2.

Estimation of the SSRT with the integration method. A, Data from the STOP trials yield an inhibition function, the probability that the monkey failed to countermand the targeting saccade (noncanceled STOP trials) as a function of stop-signal delay. B, The race model consists of a GO process (dotted line) and a STOP process (solid line) racing independently toward their respective threshold (broken horizontal line). The GO and STOP processes are initiated by the presentation of the saccade target and the stop signal, respectively. In STOP trials, the STOP process begins after the GO process has begun. If the GO process finishes first, then the saccade will not be canceled. In contrast, if the STOP process finishes before the GO process, then the saccade is canceled. The duration of this stop process is the SSRT. C, The SSRT at each SSD can be determined by integrating the distribution of the reaction times of the saccades made in the CONTROL trials, beginning at zero, until the integral equals the probability of noncanceled trials observed at each SSD. The time value at that point indicates the time that the STOP process ended. Thus, the interval from the presentation of the stop signal to this time value represents the SSRT.

Figure 3.

Activity of one SC saccade-related neuron recorded during the countermanding saccade task. Top, Activity during canceled and noncanceled STOP trials with a 170 msec stop-signal delay. Middle, Activity during corresponding CONTROL trials. Bottom, Superimposed spike density functions for matching CONTROL (gray) and STOP (black) trials. To facilitate the comparison between conditions, each panel shows the time of the stop signal presentation (thick vertical line) and the time of the behavioral estimate of saccade cancellation (broken vertical line). The neural estimate of saccade cancellation (thin vertical line) is the time at which the differential spike density function (dotted function) crossed the significance threshold (broken horizontal line). Circles indicate saccade onsets.

Figure 4.

A, Distribution of the ratios of activity in the 40 msec interval centered on the time of the behavioral estimate of saccade cancellation in canceled STOP trials and corresponding CONTROL trials for the group of trials collected in each stop-signal delay in 32 SC saccade-related neurons. Solid cells indicate the groups with activity ratios that were significantly greater than unity. B, Distribution of the timing difference between the neural and behavioral estimates of saccade cancellation for the same saccade-related neurons. Each stop-signal delay from each neuron contributed one data point.

Figure 5.

Comparison between the greatest maximum peak activation during canceled STOP trials and the maximum saccade-aligned activation during all CONTROL trials for each of the 32 SC saccade-related neurons.

Figure 6.

Distribution of the ratios of activity of SC saccade-related neurons in the 40 msec interval before saccade initiation in noncanceled STOP trials and corresponding CONTROL trials. Each stop-signal delay from each neuron contributed one data point. Solid cells indicate ratios of groups with statistically significant differences.

Figure 7.

Activity of one SC fixation-related neuron recorded during the countermanding saccade task. Top, Activity during canceled STOP trials with a 175 msec stop-signal delay and with the target presented 10° left (A-C) and 10° right (D-F) of the fixation point. Middle, Activity during corresponding CONTROL trials. Bottom, Superimposed spike density functions for matching CONTROL (gray) and STOP (black) trials. See Figure 3 legend for details.

Figure 8.

A, Distribution of the ratios of activity in the 40 msec interval centered on the time of the behavioral estimate of saccade cancellation in canceled STOP trials and corresponding CONTROL trials for the group of trials collected in each stop-signal delay in 10 SC saccade-related neurons. Solid cells indicate the groups with activity ratios that were significantly smaller than unity. B, Distribution of the timing difference between the neural and behavioral estimates of saccade cancellation for the same fixation-related neurons.