Memory Retrieval Operations Produce a Reset of Theta Oscillations in Humans

Abstract:
The high signal-to-noise ratio of human intracranial recordings presents an unprecedented opportunity to examine brain oscillations with high temporal and spatial precision. Our group has shown that these oscillations occur predominantly in the theta band and appear to be related to the cognitive demands of both spatial and non-spatial memory tasks. These results mirror the extensive literature of the role of theta in rodent learning and memory. The task dependence of theta activity raises the question of whether theta is initiated or reset by specific cognitive events. Both of these situations predict that the presentation of study and test stimuli would affect the phase of theta oscillations. We tested this hypothesis in three participants with pharmacologically resistive epilepsy who were undergoing invasive monitoring prior to possible resection surgery. Participants performed a short-term item recognition task using consonants as stimuli. In each participant we observed sites where theta significantly increased during performance of this memory task. Among these sites, many exhibited a clear alignment of theta phase following the presentation of probe items. We also observed phase alignment following study items, but this effect was significantly weaker than the probe alignment effect. These results are consistent with theta phase being reset in response to memory retrieval operations and suggests a tighter linkage between theta oscillations and cognitive demands than previously suspected.