Memory reactivation of real-world spatial orientation revealed by human electrophysiology

Spatial navigation and memory are thought to rely on common neuronal mechanisms, enabling us to travel in physical and mental space. Seminal findings in animal models support this assumption. However, how navigation and memory processes interact in humans is not well understood. Here we tested whether real-world head orientations act as spatial context for memories by investigating their reactivation during wake and sleep. We recorded intracranial electrophysiology in epilepsy patients and scalp EEG in healthy participants while they retrieved real-world head orientations as well as while targeted memory reactivation (TMR) was applied during subsequent non-rapid eye movement (NREM) sleep. We show that head orientation-related signals are reactivated during successful memory retrieval, suggesting that they provide specific memories with spatial information. Moreover, we found that TMR triggered reactivation of prior learned head orientations during sleep. Sleep related memory reactivation was paralleled and predicted by increased power in the SO-spindle range while being accompanied by elevated levels of ripples recorded intracranially from the medial temporal lobe. In conclusion, our results suggest that core features of spatial navigation add contextual spatial information to newly formed memory traces.