Hierarchical Reconfiguration of Neurocognitive Task Set Representations Mediates Cognitive Flexibility

Abstract Cognitive control organizes abstract contexts, stimuli, and actions into hierarchically structured representations. This organization supports flexible behavior but requires updating at multiple levels of the hierarchy, a process reflected in task switch costs. However, it remains unclear how updating differs across levels of abstraction and how these differences relate to behavior and neural representations. Here, we investigated the behavioral and neural sources of switch costs using fMRI and behavioral data from healthy adult participants (male and female). We employed a hierarchical control task that dissociates abstract context reconfiguration from more concrete task-set reconfiguration of stimulus-response mappings. We predicted that task sets, which incorporate sensory–motor mappings, would be more strongly influenced by feedforward inputs than higher-level contextual goals, which are more abstracted from immediate perceptual and motor demands. As predicted, subordinate rule switches were faster and were more strongly influenced by task-irrelevant perceptual changes, whereas context switches were slower and relatively insensitive to such interference. To characterize the neural basis of these effects, we quantified trial-to-trial reconfiguration of multivoxel activity patterns. Across the brain, larger pattern shifts predicted larger RT switch costs, linking representational reorganization to behavioral performance. Importantly, representational reconfiguration differed across hierarchical levels and anatomical systems. Subordinate rule updating was modulated by task-irrelevant perceptual features and expressed in distributed perceptual and motor networks, whereas context reconfiguration engaged the mid-lateral frontal cortex and was comparatively insulated from interference. Our results reveal how the hierarchical structure of neural representations supports flexible updating with interference-shielded contextual representations subserving behavioral control. Significance Daily activities often require simultaneously updating different tasks and thoughts. Driving requires maintaining a stable destination goal while rapidly updating motor plans (brake, accelerate, turn, etc.) in response to changing perceptual information (traffic lights, pedestrians, etc.). Although people perform such tasks with ease, it remains unclear how neural and cognitive representations are structured to respond to these flexibility demands. The present study suggests that sensory-motor plans prioritize flexibility by allowing greater influence from sensory inputs, which can create interference across brain networks when that input is task-irrelevant. Contextual information is insulated from this interference by representing contexts as distinctly as possible in the lateral prefrontal cortex, resulting in slower but more stable context switching. Competing Interest Statement The authors have declared no competing interest. Footnotes We have substantially revised our wording regarding the hypotheses/predictions throughout the Introduction, Methods, and Results sections in order to improve clarity. Related to this, we have modified our descriptions of analyses and results to make it more clear what analyses and contrasts were performed to test these hypotheses and support our predictions. As requested, we now also include an unbiased ROI contrast. We have also addressed the reviewers comments regarding our measure of trial-to-trial reconfiguration of neural activity patterns (formerly referred to as neural distance; henceforth referred to as pattern shifts). The Discussion section now includes requested paragraphs on potential locus of slack interpretations and how the present results coexist with our previous findings. We have also removed the error and post-error results/discussion from the Results and Discussion sections to restrict reported results to only the most critical analyses. All figures have been modified as requested by reviewers. Some minor wording and formatting changes throughout as requested by reviewers as well