Evidence That Autobiographic Memory Retrieval Does Not Become Independent of the Hippocampus: An fMRI Study Contrasting Very Recent with Remote Events

Traditional consolidation theory, which seeks to explain how new memories are incorporated into the preexisting neural architecture, stipulates that the hippocampus plays a time-limited role in this process. However, although there is abundant research showing that the hippocampus is necessary for the initial (encoding) phase, there is very little experimental evidence with human subjects proving that the structure ceases to play a role in the retrieval of episodic items from memory stores. To test this hypothesis, we investigated recall activation associated with recent memories (2.5 days) versus remote memories (mean of 8 years) using functional magnetic resonance imaging. In accordance with the multiple memory trace theory, recall of consolidated autobiographic information, represented by the remote condition, was not independent of the hippocampus. Both types of memory retrieval produced significant activation in parahippocampal, prefrontal, and midtemporal gyri, the parietal-temporal junction, and a medial region of cortex spanning the posterior cingulate and precuneus gyri. However, where recent events activated bilateral regions of the caudate nucleus, remote events yielded significantly greater activation within the hippocampus proper. The results challenge traditional consolidation theory, which would predict greater hippocampal activity for recent events. Furthermore, they highlight the interplay between multiple memory systems in the brain. We argue that our particular question format, which encouraged depth of recall and did not require a prescan interview, as well as our delineation of the recent and remote time periods, were the determining factors for the observed pattern of hippocampal activation.