Hierarchical organization of cognition reflected in distributed frontoparietal activity

Abstract

Organization of behavior into a nested hierarchy of tasks and subtasks is characteristic of purposive cognition in humans. While frontoparietal regions have been shown to represent many kinds of task events, their representation of task/subtask structure has not been directly investigated. On each trial of the current study, participants carried out a sequence of four visual target detections organized by task context into subtasks of different structure (three and one or two and two). Through extended regions of frontoparietal cortex, activity elicited by target detections depended upon the hierarchical level of the episode completed. Target detections completing the entire trial elicited greatest activity, followed by targets completing a subtask, and finally targets within one subtask. Results depended on task and subtask completion, rather than the complexity of the next task stage to be established. We suggest that, through large regions of frontoparietal cortex, control representations direct each step of a behavioral program. Completion of a subtask revises control representations related just to this subtask, leaving those related to the overarching task episode intact, while completion of the entire task revises the entire assembly of representations.

Figure 1.

a, Structure of a typical trial in Experiment 1. Trials began with a three-letter cue word. The three letters of this word were to be covertly detected, in the correct order, in the ensuing letter stream; after all three had been detected, search for the letter X began. The complete sequence of four target letters appeared in only half of the trials. The letter stream ended with a probe asking whether the letter X had appeared in the correct sequential position, i.e., following the three letters of the target word. Thus the first two targets (T1 and T2) completed subgoals at the lowest level (component letters of the first target word; level 1); the third target, T3, completed a subgoal at the next highest level (complete target word; level 2), while the fourth target, T4 (X), completed the whole goal of the task (level 3). Dotted arrows indicate the variable number of nontarget letters between initial cue, successive targets, and final probe. b, Structure of a typical trial in Experiment 2. The cue consisted of a two-letter word, the detection of which was followed by detection of the letters of word ‘MY’, the latter being constant across trials. In this scheme T1 and T3 completed a level 1 episode, T2 completed a level 2 episode, and T4 completed the whole task (level 3). c, Structure of a typical trial in Experiment 3, similar to Experiment 1 but with only three targets, T1–T3.

Figure 2.

Experiment 1. The whole brain render shows areas where target detection significantly modulated brain activity (ANOVA comparing the first 5 FIR regressors after each target detection event; results thresholded at family-wise error corrected p < 0.05). For ROIs, estimates of eight FIR regressors linked to each target event were extracted and plotted to construct the time course of BOLD activity (blue, T1; green, T2; red, T3; purple, X). L, Left; R, right.

Figure 3.

Experiment 1. Comparison of phasic activity in response to various target events. Plots show activity index for each target. This was derived for each target event by subtracting the estimate of the first FIR regressor from the average of the second and third. The error bars represent one standard error of the mean.

Figure 4.

Experiment 1. a, Whole-brain render showing areas that had higher activation index for T3 compared to T1 and T2. b, Areas with greater activity for X than T1 and T2.

Figure 5.

Experiment 2. Comparison of activity index in response to various target events. Across multiple ROIs, compared to Figure 3, note relative increase in T2 activity and decrease in T3 activity.

Figure 6.

Experiment 3. Comparison of activity index in response to the three target events. Results were closely similar to those of Experiment 1.