Neural basis of adaptive response time adjustment during saccade countermanding

Abstract

Humans and macaque monkeys adjust their response time adaptively in stop-signal (countermanding) tasks, responding slower after stop-signal trials than after control trials with no stop signal. We investigated the neural mechanism underlying this adaptive response time adjustment in macaque monkeys performing a saccade countermanding task. Earlier research showed that movements are initiated when the random accumulation of presaccadic movement-related activity reaches a fixed threshold. We found that a systematic delay in response time after stop-signal trials was accomplished not through a change of threshold, baseline, or accumulation rate, but instead through a change in the time when activity first began to accumulate. The neurons underlying movement initiation have been identified with stochastic accumulator models of response time performance. Therefore, this new result provides surprising new insights into the neural instantiation of stochastic accumulator models and the mechanisms through which executive control can be exerted.

Figure 1.

Saccade stop-signal (countermanding) task. Dotted circles indicates gaze position, and the arrow indicates the direction of the saccade. All trials began with the presentation of a central fixation spot. After a variable fixation interval, the fixation spot disappeared and, simultaneously, a target appeared at an eccentric location to the right or left of central fixation. On ∼30% of trials (stop-signal trials), the fixation spot was reilluminated after an interval (stop-signal delay) after target onset. Fixation reillumination was the cue for the monkeys to withhold a saccade to the target. Trials in which monkeys were successful in maintaining fixation were referred to as canceled trials, and trials in which monkeys made a saccade to the eccentric target were referred to as noncanceled trials. For the remaining ∼70% of trials (no-stop-signal trials), the fixation point was not reilluminated and monkeys were reinforced for making a saccade to the peripheral target.

Figure 2.

Vincentized response time distributions for no-stop-signal trials preceded by either a no-stop-signal trial (black line) or a canceled trial (gray line) for data collected in sessions during which movement cells were recorded in FEF (a) and SC (b).

Figure 3.

Time course of activity of representative movement neuron in FEF (top) and in SC (bottom) aligned on target presentation (left) and saccade initiation (right) for no-stop-signal trials preceded by either no-stop-signal (black) (FEF n = 34, SC n = 371) or canceled stop-signal (gray) (FEF n = 9, SC n = 73) trials. The onset (vertical arrow) and average RT (vertical line) are indicated for both neurons for both trial sequences.

Figure 4.

Time course of grand average of activity of FEF (top) and SC (bottom) neurons aligned on target presentation (left) and saccade initiation (right) for no-stop-signal trials preceded by either no-stop-signal (black) or canceled stop signal (gray). The discharge rates were normalized to the trigger thresholds of individual neurons. Average onset times indicated by the vertical lines. Note the common thresholds and rates of accumulation, especially in the plots aligned on saccade initiation. Also note the continuously earlier accumulation in NS-NS as compared to C-NS trials.

Figure 5.

a–d, Stacked bar plots of the differences in the threshold activity level (ΔT) (a), baseline activity level (ΔB) (b), rate of growth (Δr) (c), and time of onset of accumulation (Δo) (d) for FEF (filled) and SC (open) between no-stop-signal trials preceded by either a no-stop-signal trial or a canceled trial. Insets diagram the alternative mechanisms of RT change for no-stop-signal trials preceded by either a no-stop-signal trial (black) or a canceled trial (gray). Only the difference in time of onset of accumulation accounted for the RT difference (ΔRT).

Figure 6.

Visual responses in FEF (top) and SC (bottom) for representative neurons (left) and average (right) for no-stop-signal trials preceded by either no-stop-signal (black) or canceled (gray) trials. Average RT (vertical line) in the two trial sequences is indicated for the individual neurons.