Neural mechanisms of episodic memory formation revealed by EEG frequency tagging

Episodic memory formation entails the integration of diverse elements such as people, places, and objects. This process, known as binding, creates a unified memory trace that the brain maintains and retrieves as a coherent representation of the episode. Despite extensive research, the precise neural mechanisms underlying this binding process are still not fully understood. We hypothesized that the binding of disparate event elements into a unified representation could be reflected through the synchronization of neural oscillations at specific frequencies induced by EEG frequency tagging. Specifically, the coordination and communication between brain regions involved in binding may be captured in the interaction between distinct frequencies, manifested in the intermodulation frequency component. Frequency tagging, commonly used in perceptual research, could thus offer new insights into processes of higher-level cognitive integration. We conducted an associative memory task where participants encoded a series of events while their EEG was recorded. Each event comprised two images from different categories (places and objects), presented for 10 seconds. During encoding, the contrasts of the place and object images were modulated at distinct frequencies (6 and 7.5 Hz, respectively). Memory for all combinations of event-specific elements was subsequently tested, requiring participants to form strong associations between the elements within each event to succeed. Analysis of the steady-state visual evoked potentials during encoding indeed revealed an intermodulation component at 13.5 Hz, resulting from the sum of the two frequencies (6 + 7.5 Hz). The strength of this intermodulation component correlated with associative memory performance, being higher in participants with better memory scores. This finding indicates that the intermodulation component mirrors the element binding subserving episodic memory formation. Our study demonstrates for the first time that intermodulation during frequency tagging can reveal cognitive integration processes beyond mere perception.