Abstract

Systems-level consolidation refers to the time-dependent reorganisation of memory traces in the neocortex, a process in which the ventromedial prefrontal cortex (vmPFC) has been implicated. Capturing the precise temporal evolution of this crucial process in humans has long proved elusive. Here, we used multivariate methods and a longitudinal functional magnetic resonance imaging (fMRI) design to detect, with high granularity, the extent to which autobiographical memories of different ages were represented in vmPFC and how this changed over time. We observed an unexpected time course of vmPFC recruitment during retrieval, rising and falling around an initial peak of 8–12 months, before reengaging for older 2- and 5-year-old memories. This pattern was replicated in 2 independent sets of memories. Moreover, it was further replicated in a follow-up study 8 months later with the same participants and memories, for which the individual memory representations had undergone their hypothesised strengthening or weakening over time. We conclude that the temporal engagement of vmPFC in memory retrieval seems to be nonmonotonic, revealing a complex relationship between systems-level consolidation and prefrontal cortex recruitment that is unaccounted for by current theories.

Highlights

  • We possess a remarkable ability to retrieve, with ease, one single experience from a lifetime of memories

  • One week prior to the functional magnetic resonance imaging (fMRI) scan, with the assistance of personal photographs, participants (n = 30) verbally recalled and rated the characteristics of autobiographical memories from 8 time periods: memories that were 0.5 months old (0.5 M, i.e., 2-week-old memories), 4 M, 8 M, 12 M, 16 M, 20 M, 24 M, and 60 M old—these latter memories serving as a definitive benchmark for remote (5-year-old) memories

  • Participants created a short phrase pertaining to each autobiographical memory, which was paired with the photograph to facilitate recall during the subsequent fMRI scan

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Summary

Introduction

We possess a remarkable ability to retrieve, with ease, one single experience from a lifetime of memories. How these individual autobiographical memories are represented in the brain over time is a central question of memory neuroscience that remains unanswered. The stabilisation of new memory traces through modification of synaptic connectivity takes only a few hours [1] and is heavily dependent upon the hippocampus [2,3,4,5]. One theory asserts that the hippocampus is not involved in the retrieval of memories after they have become fully consolidated to the neocortex [7]. Alternate views maintain that vivid, detailed autobiographical memories retain a permanent reliance on the hippocampus for their expression [8,9,10,11,12]

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