An oculomotor decision process revealed by functional magnetic resonance imaging

Abstract

It is not known how the brain decides to act on moving objects. We demonstrated previously that neurons in the macaque supplementary eye field (SEF) reflect the rule of ocular baseball, a go/nogo task in which eye movements signal the rule-guided interpretation of the trajectory of a target. In ocular baseball, subjects must decide whether to pursue a moving spot target with an eye movement after discriminating whether the target will cross a distal, visible line segment. Here we identify cortical regions active during the ocular baseball task using event-related human functional magnetic resonance imaging (fMRI) and concurrent eye-movement monitoring. Task-related activity was observed in the SEF, the frontal eye field (FEF), the superior parietal lobule (SPL), and the right ventrolateral prefrontal cortex (VLPFC). The SPL and right VLPFC showed heightened activity only during ocular baseball, despite identical stimuli and oculomotor demands in the control task, implicating these areas in the decision process. Furthermore, the right VLPFC but not the SPL showed the greatest activation during the nogo decision trials. This suggests both a functional dissociation between these areas and a role for the right VLPFC in rule-guided inhibition of behavior. In the SEF and FEF, activity was similar for ocular baseball and a control eye-movement task. We propose that, although the SEF reflects the ocular baseball rule, both areas in humans are functionally closer to motor processing than the SPL and the right VLPFC. By recording population activity with fMRI during the ocular baseball task, we have revealed the cortical substrate of an oculomotor decision process.

Figure 1.

a, Baseball configuration, showing eight possible strike-zone locations, bluish fixation, and target moving from the center toward the strike zone (trajectory indicated by arrow, not part of stimulus display). b, Subjects fixate on a blue central fixation point between 0.54 and 3.46 s. The fixation point then changes color and increases in size for 1 s to inform the subject of the task to be performed. Green, Always-go; red, always-nogo; white, ocular baseball. Next, the fixation point returns to its original size and color, and a target begins to move away from this central fixation point at an average speed of 1.75°/s (see Materials and Methods). A strike zone appears in a pseudorandomly determined location 10° from the fixation point. Subjects were instructed to maintain fixation during this phase for all trial types. Three seconds after stimulus onset, a green response cue at fixation appears, informing subjects to respond. Subjects then continue to fixate or pursue for the remainder of the trial (1 s). The target never crosses the strike zone, reaching only 7° eccentricity from the fixation point.

Figure 2.

Eye movements during ocular baseball in the scanner. a, b, Two-dimensional eye trace indicating a decided-go judgment (a) and decided-nogo judgment (b). Green, Strike zone location; black, target location from beginning of target onset to end of trial; red “X,” extrapolated location for target crossing; red line, two-dimensional eye trace after the “go” cue. c, d, Horizontal eye position (h. eye pos.) and vertical eye position (v. eye pos.) for the corresponding two-dimensional eye trace over the entire trial duration is plotted in c for the decided-go trial and in d for the decided-nogo trial. The green line represents the onset of the go cue.

Figure 3.

Representative fMRI localizer activity, showing FEF and SEF activity in an axial slice from subject JB. The self-paced saccade task is more than fixation. Activation was thresholded at p < 0.001. Regions shown were more activated during self-paced saccades than during fixation.

Figure 4.

Mean amplitude (percentage of BOLD signal) for SEF and FEF ROIs in each of the four experimental conditions (decided-go, decided-nogo, always-go, and always-nogo) averaged across ROIs for all subjects. The baseline average of amplitude is represented by 0%. Error bars indicate SEM. *p < 0.05.

Figure 5.

Mean amplitude percentage of signal for the right VLPFC (a), SPL (b), SEF (c), and FEF (d) ROIs, grouped by condition for each subject. The baseline average of amplitude from a period preceding the start of a trial is represented by 0%. Asterisks indicate significance above baseline (p < 0.05).

Figure 6.

Group average of whole-brain activity indicating regions where activity is greater in the decided-nogo condition than the always-nogo condition. Functional activity is superimposed on T1 structural images in axial slices, from z = −8 to z = 64, spaced 8 mm apart. The color bar represents t values thresholded at p < 0.001, and the extent threshold = 10 voxels. Group average reveals activity in the bilateral SPL (the two parietal loci), right VLPFC (the inferior frontal loci), and right BA6 (the superior frontal loci). R-L, Right–left.