Abstract
The role of the hippocampus in declarative memory consolidation is a matter of intense debate. We investigated the neural substrates of memory retrieval for recent and remote information using functional magnetic resonance imaging (fMRI). 18 young, healthy participants learned a series of pictures. Then, during two fMRI recognition sessions, 3 days and 3 months later, they had to determine whether they recognized or not each picture using the “Remember/Know” procedure. Presentation of the same learned images at both delays allowed us to track the evolution of memories and distinguish consistently episodic memories from those that were initially episodic and then became familiar or semantic over time and were retrieved without any contextual detail. Hippocampal activation decreased over time for initially episodic, later semantic memories, but remained stable for consistently episodic ones, at least in its posterior part. For both types of memories, neocortical activations were observed at both delays, notably in the ventromedial prefrontal and anterior cingulate cortices. These activations may reflect a gradual reorganization of memory traces within neural networks. Our data indicate maintenance and strengthening of hippocampal and cortico-cortical connections in the consolidation and retrieval of episodic memories over time, in line with the Multiple Trace theory (Nadel and Moscovitch, 1997). At variance, memories becoming semantic over time consolidate through strengthening of cortico-cortical connections and progressive disengagement of the hippocampus.
Highlights
One of the most amazing features of human memory is its capacity to retain memories on a time-scale ranging from milliseconds to the many decades that cover our life span [1]
The idea that memory traces are not immediately acquired in their definitive state but rather undergo a gradual process of consolidation over time dates back to observations made by the French psychologist Theodule Ribot in 1881. He was the first to report that, after brain damage, recently acquired information was more impaired than remote memories, a phenomenon described as temporally graded amnesia or Ribot’s law
In order to clarify this issue, we investigated using functional magnetic resonance imaging, the temporal evolution of hippocampal and cortical activity underlying the retrieval of recent and remote episodic and semantic memories over a 3month period
Summary
One of the most amazing features of human memory is its capacity to retain memories on a time-scale ranging from milliseconds to the many decades that cover our life span [1]. The idea that memory traces are not immediately acquired in their definitive state but rather undergo a gradual process of consolidation over time dates back to observations made by the French psychologist Theodule Ribot in 1881. He was the first to report that, after brain damage, recently acquired information was more impaired than remote memories, a phenomenon described as temporally graded amnesia or Ribot’s law. Ribot’s temporal gradient would be due to the greater vulnerability to amnesia of episodic relative to semantic memory. The relatively better preservation of remote memory compared with recent memory in amnesic patients was linked to their semantic nature [4,5]
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