Canonical cortico-hippocampal dynamics underlie memory of navigational episodes and its early decline in aging

Successful encoding of a navigational episode entails the dynamic processing of perceptual information, time-locked to the appearance of salient landmarks and turns along the way. We hypothesized that identical navigational experiences will be represented in a similar manner across individuals and that a deviation from such canonical dynamics in the cortico-hippocampal network may underlie differences in navigational memory across individuals and its decline in aging. 76 participants (42 females) across two age groups (young: 20-30 years, aging: 50-65 years) watched 24 different 1-minute-long first-person-view virtual navigation videos in the fMRI scanner, followed by a memory question about the traveled path or destination. Canonical dynamics were defined as the averaged neural dynamics across participants during the navigation period for each brain region. First, we found that individual-to-canonical similarity (ICS) was highest in the dorsal/ventral visual streams and precuneus and was linked to informative navigational events, such as turning or landmark viewing. ICS in the medial temporal lobe (MTL) and the coordinated activity between the hippocampus and canonical cortical dynamics were strongly associated with individual spatial memory performance. Moreover, a reduction in the intersubject functional connectivity between the MTL and the canonical cortical dynamics mediated the effects of aging on cognitive performance, highlighting its role in navigation and episodic memory. Complementary to traditional time-averaged activation measures, canonical neural dynamics may be particularly revealing of how the brain processes information across spatiotemporally extended events.