SignificanceEpisodic memories detail our personally experienced past. The formation and retrieval of these memories have long been thought to be supported by a division of labor between the neocortex and the hippocampus, where the former processes event-related information and the latter binds this information together. However, it remains unclear how the 2 regions interact. We uncover directional coupling between these regions, with power decreases in the neocortex that precede and predict power increases in the hippocampus during memory formation. Fascinatingly, this process reverses during memory retrieval, with hippocampal power increases preceding and predicting neocortical power decreases. These results suggest a bidirectional flow of information between the neocortex and hippocampus is fundamental to the formation and retrieval of episodic memories.
Theta frequency oscillations in the 6-to 10-Hz range dominate the rodent hippocampal local field potential during translational movement, suggesting that theta encodes self-motion. Increases in theta power have also been identified in the human hippocampus during both real and virtual movement but appear as transient bursts in distinct high-and low-frequency bands, and it is not yet clear how these bursts relate to the sustained oscillation observed in rodents. Here, we examine depth electrode recordings from the temporal lobe of 13 presurgical epilepsy patients performing a selfpaced spatial memory task in a virtual environment. In contrast to previous studies, we focus on movement-onset periods that incorporate both initial acceleration and an immediately preceding stationary interval associated with prominent theta oscillations in the rodent hippocampal formation. We demonstrate that movementonset periods are associated with a significant increase in both low (2-5 Hz)-and high (6-9 Hz)-frequency theta power in the human hippocampus. Similar increases in low-and high-frequency theta power are seen across lateral temporal lobe recording sites and persist throughout the remainder of movement in both regions. In addition, we show that movement-related theta power is greater both before and during longer paths, directly implicating human hippocampal theta in the encoding of translational movement. These findings strengthen the connection between studies of theta-band activity in rodents and humans and offer additional insight into the neural mechanisms of spatial navigation.theta | hippocampus | navigation | spatial memory | intracranial EEG T he rodent hippocampal local field potential (LFP) is dominated by 6-to 10-Hz theta oscillations during translational movement (1, 2). Both the power (1, 3) and frequency (3-6) of theta are positively correlated with running speed. Theta oscillations might therefore encode self-motion information and contribute to the generation of spatially modulated firing patterns (7-9). A critical concern for contemporary neuroscience is to establish whether this hypothesis can be translated across species. During navigation, intracranial recordings from depth electrodes in the human hippocampus have shown that theta is more prevalent during movement than during stationary periods (10-12) and that theta power increases with movement speed (13). In addition, increases in movement-related theta power are seen across the neocortex (10,11,14). These findings support the hypothesis that human theta oscillations might encode self-motion information. However, it has also been demonstrated that human theta-band activity typically occurs in transient bursts distributed throughout movement, in contrast to the continuous high-amplitude oscillation observed in the rodent (15,16). Moreover, these studies identified movement-related oscillations within both higher and lower frequency theta bands (17)(18)(19)(20). Hence, it is not yet clear how theta oscillations in the human hippocampus relate to thos...
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