Theta oscillations in the human hippocampus normalize the information content of episodic memory

Abstract

The principles governing the formation of episodic memories from the continuous stream of sensory stimuli are not fully understood. Theoretical models of the hippocampus propose that the representational format of episodic memories comprise oscillations in the theta frequency band (2-8 Hz) that set the time boundaries in which discrete events are bound encoded in the gamma frequency range (>30 Hz). We investigated this temporal segmentation and binding process by analyzing the intracranial EEG (iEEG) of surgically implanted epileptic patients performing a virtual-navigation task. We found a positive correlation between sensory information density encountered by the subject and hippocampal theta-frequency, suggesting that the human hippocampus normalizes the information content of episodic memories relative to the density of sensory information. This interpretation is further supported by the observation that as a marker of mnemonic encoding, i.e. the amount of persistent gamma events, directly correlates with sensory information density, gamma-frequency power and the phase relation between theta and gamma oscillations remain constant. Using a theoretical model of the hippocampus, we build a model that analogously displays a similar normalization of gamma episodes per theta cycle relative to information density by accounting for the physiological signatures of theta-gamma coding through combining fast and slow inhibitory feedback. We propose that this intrinsic normalization mechanism optimizes the trade-off between the discretization and compression of continuous experience relative to the limited capacity of episodic memory. SummaryWe move in continuous time and space, yet we can encode and recall discrete episodes from our past experiences. The neural mechanism behind this discretization is not fully understood. It has been previously observed that rodent locomotion modulates ongoing hippocampal theta rhythms. Thus, raising the question of whether these slow rhythms bind events together during a single oscillatory cycle relative to the movement speed or overall information density. We quantified the effects of increasing locomotion and sensory information in modulating theta oscillations during virtual navigation with intracranial hippocampal activity from human epileptic patients.. We observed hippocampal theta waves increased with higher speed and higher sensory demands, thereby maintaining constant information per oscillatory cycle. These results highlight the role of hippocampal theta oscillations in discretizing ongoing experience relative to the available information and explain how episodic memory integrates a fixed number of items per oscillatory theta cycle irrespective of richness of the external world.