Abstract
Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. On a neural level, these 2 processes are thought to be supported by neocortical alpha/beta desynchronization and hippocampal theta/gamma synchronization, respectively. Intuitively, these 2 processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. We address this by analyzing human intracranial electroencephalogram data recorded during 2 associative memory tasks. We find that neocortical alpha/beta (8 to 20 Hz) power decreases reliably precede and predict hippocampal "fast" gamma (60 to 80 Hz) power increases during episodic memory formation; during episodic memory retrieval, however, hippocampal "slow" gamma (40 to 50 Hz) power increases reliably precede and predict later neocortical alpha/beta power decreases. We speculate that this coupling reflects the flow of information from the neocortex to the hippocampus during memory formation, and hippocampal pattern completion inducing information reinstatement in the neocortex during memory retrieval.
Highlights
Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation
Foreshadowing the results below, we show that ATL alpha/beta power decreases precede hippocampal fast gamma power increases during successful memory formation, and that hippocampal slow gamma power increases precede ATL alpha/beta power decreases during successful memory retrieval
We have demonstrated that both neocortical alpha/beta power decreases and hippocampal fast and slow gamma power increases arise during episodic memory processes
Summary
Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. These 2 processes are thought to be supported by neocortical alpha/beta desynchronization and hippocampal theta/gamma synchronization, respectively These 2 processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. Synchronizing alpha/beta rhythms via repetitive transcranial magnetic stimulation impairs both episodic memory formation and retrieval, suggesting that alpha/beta desynchronization plays a causal role in these processes [20, 25] In conjunction, these studies suggest that neocortical alpha/beta desynchronization underpins the processing of event-related information, allowing for the formation and later recollection of highly detailed episodic memories. The framework posits that these 2 mechanisms need to cooperate, as an isolated failure of either of these mechanisms would produce the same undesirable outcome: an incomplete memory trace We test this framework and uncover evidence of an interaction between neocortical desynchronization and hippocampal synchronization during the formation and retrieval of human episodic memories. This hypothesis is based on the principles of information theory [8], which proposes that a system of unpredictable states (e.g., desynchronized neural activity, where the firing of one neuron is not predictive of the firing of another; see ref. 5 for details) is optimal for information
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