Distinct neural architectures prevent off-task thought in different task contexts

Abstract

Prevailing models propose that sustained focus is a product of top-down control that amplifies task-relevant representations while suppressing distraction. We challenge this view, demonstrating that the neural signatures of mental focus differ across cognitive modes. In two neuroimaging studies, we used a paradigm that creates conflict between external task goals and self-generated thought and modelled neural activity as a function of trial-by-trial subjective focus to identify how people stay on task in contexts varying in memory engagement. In Study 1, on-task thoughts were associated with distinct neural architectures in arithmetic and comprehension: arithmetic-related focus recruited visual-motor regions, while comprehension-related focus was characterized by the recruitment of memory systems and reduced activation of control regions. Study 2 extended these findings, with both externally directed comprehension and internal memory retrieval associated with a shared neural profile of reduced control engagement, despite reliance on distinct memory systems. Furthermore, focus covaried with activity in heteromodal semantic regions across both reading and listening, suggesting semantic engagement is a primary marker of being on-task during comprehension. Our findings indicate that sustained focus during memory-guided cognition is characterized by mutual disengagement between control and memory networks. This discovery challenges the view that top-down supervision is a universal requirement for task focus, since sustained attention is associated with distinct neural configurations in different cognitive modes.