Development and decline of the hippocampal long-axis specialization and differentiation during encoding and retrieval of episodic memories

Abstract

Change in hippocampal function is a major factor in lifespan development and decline of episodic memory. Evidence indicates a long-axis specialization where anterior hippocampus is more engaged during encoding and posterior during retrieval. We tested the lifespan trajectory of hippocampal long-axis episodic memory-related activity and functional connectivity (FC). 496 participants (6.8-80.8 years) were scanned with functional MRI while encoding and retrieving associative memories. We found clear evidence for a long-axis encoding-retrieval specialization. These long-axis effects declined linearly during development and aging, eventually vanishing in the older adults. This was mainly driven by age effects on retrieval. Retrieval was associated with gradually lower activity from childhood to adulthood, followed by positive age-relationships until 70 years. Interestingly, this pattern characterized task engagement regardless of memory success or failure. Children engaged posterior hippocampus more than anterior, while anterior hippocampus was more activated relative to posterior already in teenagers. Intra-hippocampal connectivity increased during task, and this increase declined with age. In sum, the results suggest that hippocampal long-axis differentiation and communication during episodic memory tasks develop rapidly during childhood and adolescence, are markedly different in older compared to younger adults, and are related to task engagement, not the successful completion of the task.