Not all memory declines with age: Neural correlates of implicit associative memory in younger and older adults

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Abstract

While explicit associative memory declines with age, implicit associative memory remains preserved. Few studies have examined the neural basis of implicit associative memory in aging, and it remains unclear whether the hippocampus is required as it is more often associated with explicit associative memory. While undergoing functional magnetic resonance imaging, young and old adults completed a speeded object categorization task in which they viewed pictured objects with superimposed words. Implicit memory was tested by presenting intact (original pairs) and rearranged pairs (items previously presented, but not together) from encoding while participants did the same categorization task. Associative priming was defined as faster reaction times (behavioural associative priming) and less activation for intact than rearranged pairs at retrieval (neural associative priming). Whole-brain analyses revealed neural associative priming in occipitotemporal and frontal regions that did not differ by age. A region of interest analysis (using subject-specific masks of medial temporal lobe regions) showed that only older adults had greater posterior hippocampal activation to intact than rearranged items at test, though activation in the hippocampus did not relate to behavioural associative priming. In contrast, greater behavioural associative priming was related to greater neural associative priming in the perirhinal cortex in both age groups. Together, these findings suggest that implicit associative priming remains intact with age, possibly because it relies on additional processes outside the hippocampus such as perirhinal-dependent unitization.

Significance Statement

The results from this paper contribute to two debates in the field: first, whether medial temporal lobe regions, especially the hippocampus, support implicit associative memory; and second, whether associative binding is preserved with age. We show that behavioural and neural measures of implicit associative memory are comparable in younger and older adults, and that in older adults, the hippocampus and perirhinal cortex appear to support implicit associative memory. Together, these findings suggest that age-related associative deficits may reflect difficulty with explicit, intentional retrieval rather than a failure to form associations. They also suggest that the hippocampus contributes to relational memory even without conscious awareness. More broadly, this points to implicit measures as a sensitive way to assess memory in aging.

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