Neural Reinstatement and Sequential Reactivation of Navigational Episodic Memory and Its Age-related Decline

When we retrieve memories of past navigational episodes, our brain reactivates cortical representations of the spatial information experienced along the way. Although navigation is temporally dynamic in nature, previous studies on cortical memory reactivation have mostly focused on single items or associated contexts. To investigate whether sequential reactivation of navigational events can be measured from cortical electrophysiological activity and depends on the availability of spatial cues such as environmental landmarks, we designed a task in which participants were passively navigated through virtual environments and then were asked to remember the routes or destinations that they traveled to. Navigational episodes comprised of an average of 5 turns and differed in the availability of landmarks. Given the decline in navigational abilities in aging, we separately tested both younger (ages 22-32) and middle-aged participants (ages 41-63) to identify age-related differences in this memory retrieval process. Comparing EEG spectral patterns between navigational encoding and retrieval, we found that sequential reactivation of turn events was associated with successful spatial memory in younger adults. This sequential reactivation was associated with the reinstatement of neural activity during distal landmark-viewing and was significantly driven by theta and alpha oscillations. While middle-aged adults showed diminished sequential reactivation overall, those with preserved landmark reinstatement and sequential reactivation patterns exhibited better spatial memory. These results may have implications for our understanding of episodic memory retrieval beyond navigation.