Theta Phase Synchronization Is the Glue that Binds Human Associative Memory

Abstract

Episodic memories are information-rich, often multisensory events that rely on binding different elements [1]. The elements that will constitute a memory episode are processed in specialized but distinct brain modules. The binding of these elements is most likely mediated by fast-acting long-term potentiation (LTP), which relies on the precise timing of neural activity [2]. Theta oscillations in the hippocampus orchestrate such timing as demonstrated by animal studies in vitro [3, 4] and in vivo [5, 6], suggesting a causal role of theta activity for the formation of complex memory episodes, but direct evidence from humans is missing. Here, we show that human episodic memory formation depends on phase synchrony between different sensory cortices at the theta frequency. By modulating the luminance of visual stimuli and the amplitude of auditory stimuli, we directly manipulated the degree of phase synchrony between visual and auditory cortices. Memory for sound-movie associations was significantly better when the stimuli were presented in phase compared to out of phase. This effect was specific to theta (4 Hz) and did not occur in slower (1.7 Hz) or faster (10.5 Hz) frequencies. These findings provide the first direct evidence that episodic memory formation in humans relies on a theta-specific synchronization mechanism.

Functional wiring of the human medial temporal lobe

“…Theta networks of memory encoding and retrieval. Given strong evidence in the literature for synchronous memory effects in the theta band (33)(34)(35)(36)(37), we first sought to characterize the detailed structure of theta networks in the MTL. To do this, we asked whether any regions acted as "hubs" of the MTL by computing the node strength for each region, using theta PLV connection weights.…”

“…The extent to which different frequencies underlie neural synchronization in memory therefore remains an open question, though converging lines of evidence strongly suggest the most prominent connectivity effects occur at low frequencies (33)(34)(35)(36)(37). Moreover, no studies have deeply considered how observations of within-MTL synchronization reflect an experimenter's choice of connectivity metric, including those that are designed to limit the effects of volumeconducted signals that may affect connectivities measured across relatively short distances (38).…”

Does the heart forget? Modulation of cardiac activity induced by inhibitory control over emotional memories

“…Because this oscillatory dynamic was measured with EEG in the scalp of the participants, interpreting the contribution of different cortical sources may be done cautiously. Several works have shown that memory encoding and retrieval is supported by an increased synchronization of slow oscillatory activity (3-8 Hz), notably in the medial temporal lobe (Heusser, Poeppel, Ezzyat, & Davachi, 2016;Clouter, Shapiro, & Hanslmayr, 2017;Burke et al, 2014;. Alternatively, an increase of such activity in the frontal medial electrodes is also a strong correlate of the higher recruitment of cognitive control mechanisms (Cavanagh & Frank, 2014;Mückschel, Dippel, & Beste, 2017;Eschmann, Bader, & Mecklinger, 2018), that may also occur during the TNT procedure.…”

Signed Reward Prediction Errors in the Ventral Striatum Drive Episodic Memory

“…One possibility may be that RPEs 370 enhance theta phase synchronization. In line with such a view, experimentally induced theta 371 synchronization between visual and auditory modalities improved multimodal stimulus memories 372 (Clouter, Shapiro, & Hanslmayr, 2017), and theta phase synchronization in such a paradigm (as 373 measured via EEG) predicts memory performance on a trial-by-trial basis (Wang, Clouter, Chen, Shapiro, 374 & Hanslmayr, 2018) . Therefore, theta synchronization between relevant brain areas may play the role 375 of efficiently cementing memory information.…”