Distinct neural architectures of focus: Memory-related engagement is associated with control disengagement

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, to identify the neural correlates of task focus in contexts varying in memory engagement. In Study 1, arithmetic and comprehension tasks were associated with distinct neural architectures of task focus: 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 motivates a departure from traditional executive-control accounts, since task focus in meaningful contexts is associated with the recruitment of representational structures in long-term memory rather than active top-down supervision. Significance StatementDoes concentration always require effort? While traditional models suggest that sustained focus is a product of top-down executive supervision, we show that the brain employs fundamentally different architectures for focus depending on the cognitive mode. In two neuroimaging studies, focus was associated with distinct neural profiles - reduced engagement of memory systems in arithmetic, and control deactivation alongside the activation of distinct memory systems in comprehension and autobiographical recall. Heteromodal semantic regions were associated with focus during reading and listening, consistent with an association between semantic network engagement and task focus during comprehension. These findings indicate that sustained attention occurs across multiple neural configurations linked to different cognitive modes, challenging the view that top-down supervision is a universal requirement.