Hippocampal theta oscillations support successful associative memory formation

Abstract

1.Models of memory formation posit that recollection as compared to familiarity-based memory depends critically on the hippocampus, which binds features of an event to its context. For this reason, the contrast between study items that are later recollected versus those that are recognized on the basis of familiarity should reveal electrophysiological patterns in the hippocampus selectively involved in associative memory encoding. Extensive data from studies in rodents support a model in which theta oscillations fulfill this role, but results in humans results have not been as clear. Here, we employed an associative recognition memory procedure to identify hippocampal correlates of successful associative memory encoding and retrieval in patients undergoing intracranial EEG monitoring. We identified a dissociation between 2- 5 Hz and 5-9 Hz theta oscillations, by which 2-5 Hz oscillations uniquely were linked with successful associative memory in both the anterior and posterior hippocampus. These oscillations exhibited a significant phase reset that also predicted successful associative encoding, distinguished recollected from familiar items at retrieval, and contributed to reinstatement of encoding-related patterns that distinguished these items. Our results provide direct electrophysiological evidence that 2-5 Hz hippocampal theta oscillations support the encoding and retrieval of memories based on recollection but not familiarity. 2. Significance StatementExtensive fMRI evidence suggests that the hippocampus plays a selective role in recollection rather than familiarity, during both encoding and retrieval. However, there is little or no electrophysiological evidence that speaks to whether the hippocampus is selectively involved in recollection. Here, we used intracranial EEG from human participants engaged in an associative recognition paradigm. The findings suggest that oscillatory power and phase reset in the hippocampus are selectively associated with recollection rather than familiarity-based memory judgements. Furthermore, reinstatement of oscillatory patterns in the hippocampus was stronger for successful recollection than familiarity. Collectively, the findings support a role for hippocampal theta oscillations in human episodic memory.