Rudoler, J. H. | bioRxiv Science

bioRxiv2022

Searching memory in time and space

We investigated memory encoding and retrieval during a quasi-naturalistic spatial-episodic memory task in which subjects delivered items to landmarks in a desktop virtual environment and later recalled the delivered items. Transition probabilities and latencies revealed the spatial and temporal organization of memory. As subjects gained experience with the town, their improved spatial knowledge led to more efficient navigation and increased spatial organization during recall. Subjects who exhibited stronger spatial organization exhibited weaker temporal organization. Scalp-recorded electroencephalographic (EEG) signals revealed spectral correlates of successful encoding and retrieval. Increased theta power (T +) and decreased alpha/beta power (A-) accompanied successful encoding, with the addition of increased gamma (G+) accompanying successful retrieval. Logistic-regression classifiers trained on spectral features reliably predicted mnemonic success in held-out sessions. Univariate and multivariate EEG analyses revealed a similar spectral T +A-G+ of successful memory. These findings extend behavioral and neural signatures of successful encoding and retrieval to a naturalistic task in which learning occurs within a spatiotemporal context.

neuroscience↗

bioRxiv2022

Hippocampal theta and episodic memory

Computational models of rodent physiology implicate hippocampal theta as a key modulator of learning and memory (Buzsaki & Moser, 2013; J. E. Lisman & Jensen, 2013), yet human hippocampal recordings have shown divergent theta correlates of memory formation. Herweg et al. (2020) suggest that decreases in memory-related broadband power mask narrowband theta increases. Their survey also notes that thetas role in memory appears strongest in contrasts that isolate retrieval processes and when aggregating signals across large brain regions. We evaluate these hypotheses by analyzing human hippocampal recordings captured as 162 neurosurgical patients (N = 86 female) performed a free recall task. Using the irregular-resampling auto-spectral analysis to separate broad and narrow-band components of the field potential we show: 1) Broadband and narrowband components of theta exhibit opposite effects, with broadband signals decreasing and narrow-band theta increasing during successful encoding; 2) Whereas low-frequency theta oscillations increase prior to successful recall, higher-frequency theta and alpha oscillations decrease, masking thetas positive effect when aggregating across the full band; 3) Thetas effects on memory encoding and retrieval do not differ between reference schemes that accentuate local signals (bipolar) and those that aggregate across large reference (whole brain average). In line with computational models that ascribe a fundamental role for hippocampal theta in memory, our large-scale study of human hippocampal recordings shows that 3-4 Hz theta oscillations reliably increase during successful memory encoding and prior to spontaneous recall of previously studied items. Significance statementAnalyzing recordings from 162 patients we resolve a long-standing question regarding the role of hippocampal theta oscillations in the formation and retrieval of episodic memories. We show that broadband spectral changes confound estimates of narrowband theta activity, thereby accounting for inconsistent results in the literature. After accounting for broadband effects, we find that increased theta activity marks successful encoding and retrieval of episodic memories, supporting rodent models that ascribe a key role for hippocampal theta in memory function.

neuroscience↗