Age-related spatial memory differences are correlated with neural remapping in CA1 of the human hippocampus

Abstract

Older adults show declines in spatial memory, although the extent of these alterations is not uniform across the healthy older population. Here, we investigate the stability of neural representations for the same and different spatial environments in a sample of younger and older adults using high-resolution functional magnetic resonance imaging (fMRI) of the medial temporal lobe. Older adults showed, on average, lower neural pattern similarity for retrieving the same environment and more variable neural patterns compared to young adults. We also found a positive association between spatial distance discrimination and the distinctiveness of neural patterns between environments. Our analyses suggested that one source for this association was the extent of informational connectivity to CA1 from other subfields, which was dependent on age, while another source was the fidelity of signals within CA1 itself, which was independent of age. Together, our findings suggest both age-dependent and independent neural contributions to spatial memory performance. Significance StatementSpatial memory declines with age, although some older adults show little cognitive decline, even into their 80s. One important lead for age-related changes comes from electrophysiological studies of older rats, who have less stable neural representations for a spatial environment, termed "place cells." Using high-resolution fMRI targeting the human hippocampus, we demonstrate that older adults also have less stable neural representations within the same environment. Our results reveal, however, that there are both age and performance dependent differences driving these effects. While older adults, on average, showed alterations in information flow within the hippocampal circuit, better performing individuals showed more differentiated neural representations regardless of age. Together, these findings provide novel insight into the impact of age on spatial memory.