Neural substrates of working memory updating

Abstract

Working memory (WM) needs to protect current content from interference and simultaneously be amenable to rapid updating with newly relevant information. An influential model suggests these opposing requirements are met via a basal ganglia (BG) - thalamus gating mechanism that allows for selective updating of prefrontal cortex (PFC) WM representations. A large neuroimaging literature supports the general involvement of the PFC, BG, and thalamus, as well as posterior parietal cortex (PPC), in WM. However, the specific functional contributions of these regions to key sub-processes of WM updating, namely gate-opening, content substitution, and gate closing, are still unknown, as common WM tasks conflate these processes. We therefore combined functional MRI with the reference-back task, specifically designed to tease apart these sub-processes. Participants compared externally presented face stimuli to a reference face held in WM, while alternating between updating and maintaining this reference, resulting in opening vs. closing the gate to WM. Gate opening and substitution processes were associated with strong BG, thalamic and fronto-parietal activation, but - intriguingly - the same activity profile was observed for sensory cortex supporting task stimulus processing (i.e., the fusiform face area). In contrast, gate closing was not reliably associated with any of these regions. These findings provide new support for the involvement of the BG in gate opening as suggested by the gating model, but qualify the models assumptions by demonstrating that gate closing does not seem to depend on the BG, and that gate opening also involves task-relevant sensory cortex.