Abstract
The standard model of systems memory consolidation postulates two interacting memory stores: a hippocampal store that rapidly encodes new information and a neocortical store where enduring representations develop gradually over time. These theories assume that systems memory consolidation requires weeks, months, or even years to form stable neocortical engrams. Recent studies have shown that with repeated learning, the uncoupling from the hippocampus and formation of an enduring neocortical engram can ensue within a single learning session, especially if the learning material is already embedded into pre-existing schemas (Brodt et al., 2016, 2018). In the present study, we used functional and diffusion-weighted MRI to investigate where and when participants form content-specific cortical memory engrams of complex naturalistic stimulus material. To this end, 40 healthy participants repeatedly watched and freely recounted four movie clips that were either set in a restaurant or at an airport. Using representational similarity analysis, we were able to discriminate the different narrative contexts in functional MRI data recorded from the posterior parietal cortex (PPC) and the hippocampus. Moreover, with repeated encoding and retrieval, the PPC showed increased activity in univariate analyses when processing the memory content. Notably, we observed an increase in content- specific discriminability over learning repetitions in the precuneus, indicating a gradual strengthening of stable neocortical mnemonic representations and a decrease in content separability in the hippocampus. In diffusion MRI data, which we used to image microstructural brain plasticity in human grey matter (Sagi et al, 2012), we found that a physical memory trace formed rapidly in the parietal cortex during repeated encoding and retrieval of the complex episodic narratives and was maintained for at least 24 hours after learning. Remarkably, we could discriminate the narrative contexts in which the movies were set based on these microstructural changes in the PPC. Both functional and structural brain changes were related to how many details participants remembered about the narratives. Thus, our findings suggest that the PPC rapidly forms stable content-specific memory traces of complex narratives from the outset of learning fulfilling all criteria for a memory engram: they (i) directly relate to the learnt content, (ii) cause a change in the underlying neural substrate, (iii) predict memory retention at the behavioural level, and (iv) can be observed while lying dormant between times of active processing (Josselyn et al., 2015; Semon, 1921).
