Spontaneous Pre-encoding Activation of Neural Patterns Predicts Memory

It is well-established that whether information will be remembered or not depends on the extent to which the learning context is reinstated during post-encoding rest and/or at retrieval. It has yet to be determined, however, if the fundamental importance of reinstatement to memory extends to periods of spontaneous neurocognitive activity prior to learning. We thus asked whether memory performance can be predicted by the extent to which spontaneous pre-encoding neural patterns resemble patterns elicited during encoding. Individuals studied and retrieved lists of words while undergoing fMRI-scanning. Multivoxel hippocampal patterns during resting periods prior to encoding resembled hippocampal patterns at encoding most strongly for items that were subsequently remembered. Furthermore, across subjects, the magnitude of similarity correlated with a behavioural measure of episodic recall. The results indicate that the neural scaffold of a memory trace is spontaneously laid even before ever perceiving the to-be-encoded information. Significance Statement It is well-established that memory performance depends on the degree to which the learning-context is reinstated during post-learning rest or during retrieval. However, does memory also depend on the context prior to learning—namely, on processes occurring spontaneously before ever perceiving the to-be-learned information? To answer this question, we scanned participants using fMRI while they were learning and recalling word-lists and, crucially, also during resting periods before each list. Patterns of brain activity in memory-related regions which were elicited spontaneously during these resting periods resembled patterns during learning. Furthermore, the greater this resemblance, the better was memory performance. We demonstrate that memory can be predicted by the degree to which patterns of neural activity prior to learning are reinstated during learning.