Computational models of rodent physiology implicate hippocampal theta as a key modulator of learning and memory (Buzsáki and Moser, 2013; Lisman and 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 the theta oscillations appear most prominently in contrasts that isolate memory 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 (IRASA) to separate broad and narrowband components of the field potential, we show that (1) broadband and narrowband components of theta exhibit opposite effects, with broadband signals decreasing and narrowband theta increasing during successful encoding; (2) whereas low-frequency theta oscillations increase before successful recall, higher-frequency theta and alpha oscillations decrease, masking the positive effect of theta when aggregating across the full band; and (3) the effects of theta on memory encoding and retrieval do not differ between reference schemes that accentuate local signals (bipolar) and those that aggregate signals globally (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 before spontaneous recall of previously studied items.SIGNIFICANCE STATEMENTAnalyzing recordings from 162 participants, 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.

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 suggests that theta's role in memory appears strongest in contrasts that isolate associative retrieval processes and when aggregating signals across large brain regions. We evaluate these hypotheses by analyzing human hippocampal recordings captured as 161 neurosurgical patients 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 theta's positive effect when aggregating across the full band; 3) Theta's 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.

We investigated memory encoding and retrieval during a hybrid spatial- episodic memory task in which subjects delivered items to landmarks in a virtual environment and later recalled the delivered items. Conditional probabilities of recall transitions revealed spatial and temporal organization of studied items. We asked whether neural signatures of successful encoding and retrieval uncovered in traditional word-list paradigms also appear when learning occurs within a spatiotemporal context under conditions that interpose a navigation task between each item encoding event. We found that increased theta (+T) and decreased alpha/beta (-A) accompanied successful encoding events, with the addition of increased gamma (+G) for retrieval events. Logistic-regression classifiers trained on these spectral features reliably predicted encoding and retrieval success in "hold out" sessions. Both univariate and multivariate analyses of EEG data revealed a similar spectral T+A−G+ of successful encoding and retrieval.