Hippocampal Theta and Episodic Memory

Abstract

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.

Morpho-electric and computational properties of three types of human hippocampal CA1 pyramidal neurons

“…The resonance frequency of h CA1 pyramidal neurons (2.9 Hz) we uncovered in single neuron recordings closely matches the in vivo theta rhythm of human hippocampus (i.e. 1-4 Hz, 17,19,57 . The temporal domain at which human hippocampus operates is thus slower compared to rodents as theta-rhythm in mice and rats occur at higher frequencies (i.e.…”

“…Interestingly, the theta rhythm is the only oscillatory brain rhythm that inversely scales with brain size across mammals, in contrast to alpha, beta and gamma rhythms, which are similar across mammalian brains 16,17 . In human hippocampus, theta rhythm is 1 -4 Hz [16][17][18][19] compared to 4 -10 Hz in rats 2,20 .…”

“…Interestingly, the theta rhythm is the only oscillatory brain rhythm that inversely scales with brain size across mammals, in contrast to alpha, beta and gamma rhythms, which are similar across mammalian brains 16,17 . In human hippocampus, theta rhythm is 1 – 4 Hz 16–19 compared to 4 – 10 Hz in rats 2,20 . A slower theta rhythm directly impacts theories on human brain function, since the slower cycle could allow an increased number of neuronal assemblies to interact and lock to the same cycle 16 .…”

Intracranial neurophysiological correlates of rumination

“…We conducted a more naturalistic, self-constraint autobiographical memory task. Rudlor and colleagues ( 83 ) recently showed that this theta power reduction may be associated with broadband activity. The specific experimental design of the present study may allow for a more comprehensive and dynamic test of this notion.…”

Neural correlates of memory in a naturalistic spatiotemporal context

“…Subsequent studies have replicated the alpha decreases and gamma increases in large subject samples (Burke et al, 2014), but the theta increases have been somewhat elusive (Herweg, Solomon, & Kahana, 2020) except for studies that either specifically focused on the lowest frequencies within the theta band (Lin et al, 2017) or studies that separated narrowband and broadband components (Rudoler, Herweg, & Kahana, 2022). Studies of episodic recollection have observed similar spectral patterns of retrieval success.…”