Non-monotonic recruitment of ventromedial prefrontal cortex during remote memory recall

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 MRI 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 re-engaging for older two and five year old memories. This pattern was replicated in two independent sets of memories. Moreover, it was further replicated in a follow-up study eight months later with the same participants and memories, where 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 non-monotonic, revealing a complex relationship between systems-level consolidation and prefrontal cortex recruitment that is unaccounted for by current theories.\n\nAuthor SummaryOur past experiences are captured in autobiographical memories which allow us to recollect events from our lives long after they originally occurred. A part of the brains frontal lobe, called the ventromedial prefrontal cortex or vmPFC, is known to be important for supporting autobiographical memories especially as memories become more remote. The precise temporal profile of the vmPFCs involvement is unclear, yet this information is vital if we are to understand how memories change over time and the mechanisms involved. In this study we sought to establish the time-course of vmPFC engagement in the recollection of autobiographical memories while participants recalled memories of different ages during functional magnetic resonance imaging (fMRI). Using a method that detects brain activity patterns associated with individual memories, we found that memory-specific neural patterns in vmPFC became more distinct over the first few months after a memory was formed, but then this initial involvement of vmPFC subsided after one year. However, more remote memories (two years and older), appeared to re-engage vmPFC once again. This temporal profile is difficult to accommodate within any single existing theory. Consequently, our results provoke a re-think about how memories evolve over time and the role played by the vmPFC.