Supplementary eye field activity reflects a decision rule governing smooth pursuit but not the decision

Abstract

Animals depend on learned rules to guide their actions. Prefrontal (PFC) and premotor (PMC) cortex of primates have been reported to display rule-related neural activity, but it is unclear how signals encoded here are utilized to enforce the decision to act. The supplementary eye field (SEF) is a candidate for enforcing rule-guided ocular decisions because the activity of neurons here is correlated with the rule in an ocular decision-making task and because this area is anatomically more proximal to movement structures than PFC and PMC and receives inputs from them. However, in the previous work, the rule encoding and ocular outcome were confounded, leaving open the question of whether SEF activity is related to the rule or the behavior. In the present study, we attempted to discriminate between these alternatives by increasing task difficulty and forcing errors, thereby putting the stimulus and the behavior at odds. Single SEF neurons were recorded while monkeys performed the task in which the rule is to pursue a moving target if it intersects a visible square and maintain fixation if it does not. A delay period was imposed to monitor neural activity while the target approached the square. Two complementary populations of go and nogo neurons were found. When task difficulty was increased, the monkeys made more errors, and the neurons took longer to encode the rule. However, in error trials, most neurons continued to reflect the rule rather the monkey's ocular decision in both the delay period and after square intersection (movement period). This was the case for both directionally tuned and nondirectional SEF neurons. The results suggest that SEF neurons encode the ocular decision rule but that the decision itself likely occurs in a different structure that sums rule information from the SEF with information from other areas.

Fig. 1.

The delayed ocular go/nogo paradigm. A: temporal schematic. The square and fixation point stayed on for the duration of the trial. The target appeared 500 ms after fixation acquisition and moved at a constant angle and velocity. The time period before square intersection is defined as the delay period and the time period after that the movement period. B: spatial schematics of the target-square relationship. In each trial, a target appeared either left or right 20° in the periphery and moved from the periphery with 1 of the 4 possible angles relative to horizontal meridian. The target moved in 40° (easy nogo) and 30° (difficult nogo) and missed the square, and in others, it moved in 10° (easy go) and 20° (difficult go) and intersected the square. C: spatial schematic for extremely difficult trials. The target moved in higher radial velocity (40°/s) and in 22° (extremely difficult go) and 25° angle (extremely difficult nogo).

Fig. 2.

Eye movements recorded from example blocks of ocular go/nogo trials. Blue traces indicate success trials and red traces decision errors. A: eye position traces in easy, difficult, and extremely difficult go trials. Catch-up saccades were removed from the velocity traces. B: corresponding radial eye velocity traces in easy, difficult, and extremely difficulty go trials shown above. The small spikes shown before square intersection are microsaccades that did not bring the gaze outside of the 4 × 4° fixation window. C: eye position traces for nogo trials. D: radial eye velocity traces in nogo trials.

Fig. 3.

Behavioral outcomes in ocular no/nogo obtained from all 3 monkeys. A: movement initiation time relative to square intersection in all go success trials. Error bars indicate SEs. B: percentages of successes and errors in go and nogo trials and their SEs. Not shown here are the percentages of trials where the monkey failed to acquire the fixation point or initiated the eye movement prematurely.

Fig. 4.

Locations and depths of rule-related neurons and evoked saccade sites. The symbols indicate sites from which go (●) and nogo (○) neurons were recorded. , evoked saccade sites were located with 50–75 μA current. A: topographic map of recorded sites from monkey VC. The center of the map corresponds to the chamber center as indicated in the inset in the upright corner, which was centered 24 mm anterior and on the midline. Symbols are offset slightly if they were recorded from the same electrode track. Positive x and y axis values indicate anterior and right locations, and negative values indicate posterior and left. B: horizontal positions and measured depths of recording sites obtained from monkey VC. The coronal schematic of probed sites is based on a reference histological slice close to the center of the supplementary eye field (SEF) chamber.

Fig. 5.

Neural activity recorded from example go and nogo neurons in easy, difficult, and extremely difficult trials. Each curve represents the mean spike rate for targets of a specific motion trajectory (green: go; red: nogo). Same-color dashed lines indicate corresponding square intersection times. The arrows below the panels indicate the separation time for all go and nogo trials with the mean spike rate of all trajectories pooled. A: mean spike rates of a typical go neuron in easy go and nogo trials. B: mean spike rates of a typical nogo neuron in easy trials. C: mean spike rates of the same go neuron in difficult trials. D: mean spike rates of the same nogo neuron in difficult trials. E: mean spike rates of a go neuron in extremely difficult trials. F: mean spike rates of a nogo neuron in extremely difficult trials.

Fig. 6.

Cumulative curves of separation times for all neurons in easy and difficult trials (thick solid: go neurons in easy trial; thick dashed: nogo neurons in easy trials; thin solid: go neurons in difficult trials; thin dashed: nogo neurons in difficult trials). The corresponding vertical lines indicate the timing of square intersection. Arrows at bottom indicate the median separation times for corresponding conditions. Note that most neurons encoded go/nogo activity before square intersection even in difficult trials. Results from extremely difficult trials are not shown here because all but 1 neuron had a separation before square intersection.

Fig. 7.

Directionality of SEF activity. A: mean spike rates for all target trajectories in the delay period (left) and in the movement period (right) for an example go neurons that were not directionally tuned. B: mean spike rates for all trajectories for a directionally tuned nogo neuron. C: directionality index (DI) values for all neurons in standard go/nogo trials the delay (left) and movement periods (right). D: DI values for all neurons in the extremely difficult go/nogo trials.

Fig. 8.

Choice probability for SEF neurons. A: the frequency distributions of mean spike rate in a 25 ms interval for individual trials obtained from a go neuron, sorted by the subsequent behavioral choice. Results from easy, difficulty and extremely difficult trials were plotted separately. B: the receiver operating characteristics (ROC) functions derived by plotting the proportion of correct pursuits against the proportion of incorrect pursuits predicted by different criterion spike rates, and the area under each curve yields the choice probability (CP). C: CP in easy, difficult, and extremely difficult trials in the delay period. D: CP results in the movement period.

Fig. 9.

Neural activity in success and decision error trials. A: spike rate in go error (dashed green), go success (green), and nogo success (red) trials recorded from a go neuron in difficult trials. The vertical line indicates the corresponding square intersection times for go and nogo trials, and the black arrow indicates the separation time for go decision error and nogo success trials. The shaded area indicates the delay period with which the mean spike rate of these types of trials is compared in Fig. 8C. B: spike rate in success and go errors trials recorded from a nogo neuron in difficult trials. C: the mean spike rate of go and nogo neurons in error trials in the delay period that was normalized against that in go-success and nogo-success trials in the delay period (see methods). Bars pointing to the right indicate that the spike rate is more similar to that in go success trials, thus consistent with the rule; left-pointing bars indicate that the activity is consistent with the behavioral choice. The dashed vertical lines indicate the normalized go rate for success go (green) and nogo (red) trials. D: the normalized mean spike rate of go and nogo neurons in error trials in the movement period.