Abstract
SummaryA progressive loss of navigational abilities in old age has been observed in numerous studies, but we have only limited understanding of the neural mechanisms underlying this decline [1]. A central component of the brain’s navigation circuit are grid cells in entorhinal cortex [2], largely thought to support intrinsic self-motion-related computations, such as path integration (i.e., keeping track of one’s position by integrating self-motion cues) [3, 4, 5, 6]. Given that entorhinal cortex is particularly vulnerable to neurodegenerative processes during aging and Alzheimer’s disease [7, 8, 9, 10, 11, 12, 13, 14], deficits in grid cell function could be a key mechanism to explain age-related navigational decline. To test this hypothesis, we conducted two experiments in healthy young and older adults. First, in an fMRI experiment, we found significantly reduced grid-cell-like representations in entorhinal cortex of older adults. Second, in a behavioral path integration experiment, older adults showed deficits in computations of self-position during path integration based on body-based or visual self-motion cues. Most strikingly, we found that these path integration deficits in older adults could be explained by their individual magnitudes of grid-cell-like representations, as reduced grid-cell-like representations were associated with larger path integration errors. Together, these results show that grid-cell-like representations in entorhinal cortex are compromised in healthy aging. Furthermore, the association between grid-cell-like representations and path integration performance in old age supports the notion that grid cells underlie path integration processes. We therefore conclude that impaired grid cell function may play a key role in age-related decline of specific higher-order cognitive functions, such as spatial navigation.
Highlights
We found significant grid-cell-like representations in entorhinal cortex of young adults (Figure 2A)
We have demonstrated here that grid-cell-like representations in the human entorhinal cortex are compromised in old age
Given that grid cells play a central role in higher order cognitive functions, these findings imply that deficient grid cell firing might be a key mechanism that could mediate cognitive deficits in old age
Summary
A progressive loss of navigational abilities in old age has been observed in numerous studies, but we have only limited understanding of the neural mechanisms underlying this decline [1]. Association between Grid-Cell-like Representations and Path Integration Performance in Older Adults When combining data from both the fMRI and the path integration experiment, we found that, within the group of older adults, those participants with a higher magnitude of grid-cell-like representations showed lower path integration errors (Figure 3E) This was indicated by a significant correlation between grid-celllike representation magnitudes of older adults and their path integration errors in the body-based modality (r = À0.54; p = 0.011). In compromised grid cell systems (as more likely to be present in older adults), fundamental computations of positional information might be impaired, resulting in a direct relationship between the degree of impairment and path integration performance To further test this assumption, we split up the group of young adults using cluster analysis to identify three subgroups of participants with low, middle, and high magnitudes of grid-cell-like representations (see STAR Methods). Whereas these analyses need to be treated with caution due to the small group sizes, they support the theoretical assumption that an association between grid-cell-like representations and path integration performance is only seen when grid-cell-like representations are compromised
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