Phase-locking within human mediotemporal lobe predicts memory formation

Lesion and imaging studies have demonstrated that encoding of declarative memories, i.e. consciously accessible events and facts, is supported by processes within the rhinal cortex and the hippocampus, two substructures of the mediotemporal lobe (MTL). Successful memory formation has, for instance, been shown to be accompanied by the rhinal N400 component, followed by a hippocampal positivity, as well as by transient rhinal-hippocampal phase synchronization. However, it has been an open question, which mediotemporal electroencephalogram (EEG) measures predict memory formation most accurately. Therefore, we analyzed and compared the association of different mediotemporal EEG measures with successful memory formation. EEG characteristics were extracted from intracranial rhinal and hippocampal depth recordings in 31 epilepsy patients performing a continuous word recognition paradigm. Classical event-related potential measures, rhinal-hippocampal synchronization, as well as inter-trial phase-locking and power changes within rhinal cortex and hippocampus were evaluated. We found that inter-trial phase-locking is superior to other EEG measures in predicting subsequent memory. This means that memory formation is related to the precise timing of EEG phases within the MTL with respect to stimulus onset. In particular, early rhinal and hippocampal phase-locking in the alpha/beta range reaching its maximum already between 100 and 300 ms after stimulus onset appears to be a precursor of successful memory formation. Our data suggest that early mediotemporal phase adjustments constitute a relevant mechanism underlying declarative memory encoding.