Successful memory formation is driven by contextual encoding in the core memory network

To understand how memories are successfully formed, scientists have compared neural activity during the encoding of subsequently remembered and forgotten items. Though this approach has elucidated a network of brain regions involved in memory encoding, this method cannot distinguish broad, non-specific signals from memory specific encoding processes, such as associative encoding. Associative encoding, which is a key mechanism of learning, can be seen in the tendency of participants to successively recall, or cluster, study neighbors. We assessed the electrophysiological correlates of associative processing by comparing intracranially recorded EEG activity during the encoding of items that were subsequently recalled and clustered; recalled and not clustered; or not recalled. We found that high frequency activity (HFA) in left prefrontal cortex, left temporal cortex and hippocampus increased during the encoding of subsequently recalled items. Critically, the magnitude of this effect was largest for those recalled items that were also subsequently clustered. HFA temporally dissociated across regions, with increases in left prefrontal cortex preceding those in hippocampus. Furthermore, late hippocampal HFA positively correlated with behavioral measures of clustering. These results suggest that associative processes linking items to their spatiotemporal context underlie the traditionally observed subsequent memory effect and support successful memory formation.