Hippocampal theta and episodic memory

Abstract

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.