Figure 4. Single trial relationship of neural activity to information seeking behavior to resolve punishment uncertainty, and summary of ACC-vlPFC circuit.

(A) During Cue1 and subsequent cue presentations monkeys were allowed to gaze freely; their gaze had no influence on the outcome. As shown previously (White et al., 2019), gaze during the informative block is attracted to the location of the upcoming informative cue before it appeared to resolve reward uncertainty (top, thick red line). Crucially, anticipatory gaze also reflected attitudes to information to resolve punishment uncertainty. Monkey 1 (left) had prominent information-anticipatory gaze during punishment uncertainty (thick cyan line; summary in bar plots below). In contrast, Monkey 2 (right) only had prominent information-anticipatory gaze during reward uncertainty. In fact, Monkey 2 had more anticipatory gaze on no-outcome trials (gray) than uncertain punishment trials (p < 0.05, signed-rank test). Error bars indicate SEM. Gray bar below the x axis is the analysis time window (100 milliseconds before uncertainty resolution). (B) Difference in each neuron’s information anticipation index for uncertain punishments, when computed using trials with high vs. low anticipatory gaze. Dot and error bars above histogram indicate mean and SEM pooling all neurons; *** indicates significant difference from 0 (p < 0.001, signed-rank test). Mean and SEM for each area and each monkey are also shown. Pooled across areas, both monkeys had significant effects (p < 0.001). Monkey 2 had significantly stronger effects (p < 0.01, rank-sum test) consistent with the greater trial-to-trial variability this monkey displayed in gaze behavior (A). Pooled across monkeys, both areas had significant effects (p < 0.001) with no difference between areas (p = 0.22, rank-sum test). Inset: Neural firing rate discrimination between punishment uncertainty trials that had high vs. low anticipatory gaze, based on separate calculations for each punishment condition (Methods). (C) Summary of the ACC-vlPFC circuit coding for information seeking to resolve reward and punishment uncertainty. Anatomical and functional connections with the basal ganglia are based on our previous work showing that the basal ganglia, in particular the internal capsule bordering dorsal striatum (White et al., 2019), controls gaze shifts to seek advance information about uncertain rewards. Size of circles do not denote % of neurons within each region.