Decoding EEG for optimizing naturalistic memory

• Published in: Journal of neuroscience methods 2024-10, Vol.410, p.110220, Article 110220
• Main Authors: Rudoler, Joseph H., Bruska, James P., Chang, Woohyeuk, Dougherty, Matthew R., Katerman, Brandon S., Halpern, David J., Diamond, Nicholas B., Kahana, Michael J.
• Format: Article
• Language: English
• Subjects: Closed-loop; EEG; Episodic memory; Machine learning; Neural decoding
• ISSN: 0165-0270; 1872-678X; 1872-678X
• DOI: 10.1016/j.jneumeth.2024.110220

Spectral features of human electroencephalographic (EEG) recordings during learning predict subsequent recall variability. Capitalizing on these fluctuating neural features, we develop a non-invasive closed-loop (NICL) system for real-time optimization of human learning. Participants play a virtual navigation-and-memory game; recording multi-session data across days allowed us to build participant-specific classification models of recall success. In subsequent closed-loop sessions, our platform manipulated the timing of memory encoding, selectively presenting items during periods of predicted good or poor memory function based on EEG features decoded in real time. The induced memory effect (the difference between recall rates when presenting items during predicted good vs. poor learning periods) increased with the accuracy of neural decoding. This study demonstrates greater-than-chance memory decoding from EEG recordings in a naturalistic virtual navigation task with greater real-world validity than basic word-list recall paradigms. Here we modulate memory by timing stimulus presentation based on noninvasive scalp EEG recordings, whereas prior closed-loop studies for memory improvement involved intracranial recordings and direct electrical stimulation. Other noninvasive studies have investigated the use of neurofeedback or remedial study for memory improvement. These findings present a proof-of-concept for using non-invasive closed-loop technology to optimize human learning and memory through principled stimulus timing, but only in those participants for whom classifiers reliably predict out-of-sample memory function. •Classifiers decoded successful vs. unsuccessful memory function from scalp EEG.•Decoded neural features determined the timing of stimulus presentation.•Memory improvement depended on the accuracy of the underlying classifiers.