Dynamic Trial-by-Trial Recoding of Task-Set Representations in the Frontoparietal Cortex Mediates Behavioral Flexibility

Abstract

Cognitive flexibility forms the core of the extraordinary ability of humans to adapt, but the precise neural mechanisms underlying our ability to nimbly shift between task sets remain poorly understood. Recent functional magnetic resonance imaging (fMRI) studies employing multivoxel pattern analysis (MVPA) have shown that a currently relevant task set can be decoded from activity patterns in the frontoparietal cortex, but whether these regions support the dynamic transformation of task sets from trial to trial is not clear. Here, we combined a cued task-switching protocol with human (both sexes) fMRI, and harnessed representational similarity analysis (RSA) to facilitate a novel assessment of trial-by-trial changes in neural task-set representations. We first used MVPA to define task-sensitive frontoparietal and visual regions and found that neural task-set representations on switch trials are less stably encoded than on repeat trials. We then exploited RSA to show that the neural representational pattern dissimilarity across consecutive trials is greater for switch trials than for repeat trials, and that the degree of this pattern dissimilarity predicts behavior. Moreover, the overall neural pattern of representational dissimilarities followed from the assumption that repeating sets, compared with switching sets, results in stronger neural task representations. Finally, when moving from cue to target phase within a trial, pattern dissimilarities tracked the transformation from previous-trial task representations to the currently relevant set. These results provide neural evidence for the longstanding assumptions of an effortful task-set reconfiguration process hampered by task-set inertia, and they demonstrate that frontoparietal and stimulus processing regions support "dynamic adaptive coding," flexibly representing changing task sets in a trial-by-trial fashion.SIGNIFICANCE STATEMENT Humans can fluently switch between different tasks, reflecting an ability to dynamically configure "task sets," rule representations that link stimuli to appropriate responses. Recent studies show that neural signals in frontal and parietal brain regions can tell us which of two tasks a person is currently performing. However, it is not known whether these regions are also involved in dynamically reconfiguring task-set representations when switching between tasks. Here we measured human brain activity during task switching and tracked the similarity of neural task-set representations from trial to trial. We show that frontal and parietal brain regions flexibly recode changing task sets in a trial-by-trial fashion, and that task-set similarity over consecutive trials predicts behavior.

Keywords: cognitive control; cognitive flexibility; fMRI; frontoparietal cortex; representational similarity analysis; task switching.

Figure 1.

Experimental protocol and behavior. A, On each trial of a cued task-switching paradigm, subjects were cued to perform either a face task (decide whether the face shown is male or female) or a house task (decide whether the house shown is a one-story house or a two-story house) on stimuli consisting of semitransparent, overlaid face and house pictures. B, Mean reaction time and accuracy rates (± mean SE) are displayed as a function of trial types (switch, repeat) and CTI. ACC, Accuracy.

Figure 2.

Predicted and observed patterns of ROI-based representational dissimilarities. A, A graphical depiction of the predicted pattern of neural representational dissimilarities (or distances) between the four possible trial types: FR, FS, HR, and HS. Displacement to the left or right along the horizontal axis from the point of origin reflects the adoption of an increasingly stable/reliable representation of the face task set or house task set, respectively. The assumed dissimilarities of neural patterns are reflected in the length of horizontal arrows between conditions, where a longer line represents greater neural pattern dissimilarity. Roman numerals are used to denote distances between different pairs of conditions (see Generating predictions for neural representations and Using RSA to track task-set transformation). B, The observed mean neural pattern dissimilarities (± mean SE), averaged across ROIs, are shown for the cue and target phase, respectively, for each condition pairing. HR–HS, house repeat–house switch distance (i); FR–HR, face repeat–house repeat distance (ii); FS–HR, face switch–house repeat distance (iii); FR–HS, face repeat–house switch distance (iv); FS–HS, face switch–house switch distance (v); FR–FS, face repeat–face switch distance (vi). *p < 0.05.

Figure 3.

Brain regions encoding task-set representations. Three-dimensional surface rendering of brain regions from which whole-brain searchlight MVPA could decode the currently relevant task set at above-chance accuracy (corrected for multiple comparisons). The t scores, voxel numbers, and MNI coordinates are listed in Table 1. FG, Fusiform gyrus; IFJ, inferior frontal junction; IFG, right inferior frontal gyrus; IPL, inferior parietal lobule.

Figure 4.

Task-set classification as a function of task-repeat versus task-switch trials. A, Mean distance to the hyperplane (± mean SE) as a function of trial type (task repeat vs switch) is displayed for each ROI. See Table 2 for specific t and p values. B, Mean task-set classification accuracy as a function of trial type (task repeat vs switch) is displayed for each ROI. See Table 3 for specific t and p values. FG, Fusiform gyrus; IFG, right inferior frontal gyrus; IFJ, inferior frontal junction; L, left; R, right. *p < .05, **p < 0.01, ***p < 0.001.

Figure 5.

Mean neural pattern similarity across consecutive trials. Bars display the neural pattern correlations (± mean SE) between consecutive trials as a function of whether they were repeat or switch trials for each ROI. See Table 4 for specific t and p values quantifying these pattern dissimilarities with group-level paired-sample t tests. **p < 0.01, ***p < 0.001. FG, Fusiform gyrus; IPL, inferior parietal lobule; IFG, right inferior frontal gyrus; IFJ, inferior frontal junction; L, left; R, right.

Figure 6.

Brain regions encoding stimulus feature representations. A, 3D surface rendering of brain regions from which whole-brain searchlight MVPA could decode whether the face feature of a current stimulus was male or female at above-chance accuracy (corrected for multiple comparisons). B, 3D surface rendering of brain regions from which whole-brain searchlight MVPA could decode whether the house feature of a current stimulus was a one-story or a two-story house at above-chance accuracy (corrected for multiple comparisons).