Hippocampal Theta and Episodic Memory

Computational models of rodent physiology implicate hippocampal theta as a key modulator of learning and memory (Buzsaki and Moser, 2013; Lisman and Jensen, 2013), yet human hippocampal recordings have shown divergent theta corre-lates of memory formation. Herweg et al. (2020) suggest that decreases in memory-related broadband power mask narrow -band 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 analyz-ing 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 refer-ence 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.

Automated summary

Computational models suggest that hippocampal theta plays a crucial role in learning and memory, but human hippocampal recordings show divergent results. Decreases in memory-related broadband power mask narrowband theta increases. Theta oscillations appear prominently in memory retrieval processes and when aggregating signals across large brain regions. The study analyzed human hippocampal recordings from 162 neurosurgical patients performing a free recall task and found that broadband theta signals decrease while narrowband theta signals increase during successful encoding. Low-frequency theta oscillations increase before recall, but higher-frequency theta and alpha oscillations decrease, masking the positive effect of theta when aggregating across the full band. The effects of theta on memory encoding and retrieval are consistent regardless of the reference scheme used.