Theta power and theta-gamma coupling support long-term spatial memory retrieval.

Umesh Vivekananda,Matthew C Walker,Neil Burgess,Roman Rodionov,Anna Miserocchi,Sallie Baxendale,Daniel Bush,Fahmida A Chowdhury,James A Bisby,Beate Diehl,Andrew W Mcevoy

doi:10.1002/hipo.23284

Umesh Vivekananda, Matthew C Walker + Show 9 more

Open Access

https://doi.org/10.1002/hipo.23284

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Abstract

Hippocampal theta oscillations have been implicated in spatial memory function in both rodents and humans. What is less clear is how hippocampal theta interacts with higher frequency oscillations to support long‐term memory. Here we asked 10 presurgical epilepsy patients undergoing intracranial EEG recording to perform a long‐term spatial memory task in desktop virtual reality and found that increased theta power in two discrete bands (“low” 2‐5 Hz and “high” 6‐11 Hz) during cued retrieval was associated with improved task performance. Similarly, increased coupling between “low” theta phase and gamma amplitude during the same period was associated with improved task performance. Finally, low and high gamma amplitude appeared to peak at different phases of the theta cycle; providing a novel connection between human hippocampal function and rodent data. These results help to elucidate the role of theta oscillations and theta‐gamma phase‐amplitude coupling in human long‐term memory.

Highlights

Oscillations in the local field potential (LFP) reflect synchronous neural activity and are a likely candidate to integrate functional brain regions across multiple spatiotemporal scales (Fries et al, 2007; Buzsáki and Schomburg, 2015)
The hippocampal theta rhythm appears to make a functional contribution to both processes, with increased theta power and mesial temporal connectivity observed during episodic memory formation (Lega et al, 2012)
Separate low (2-5 Hz) and high (6-11 Hz) theta bands have been observed during short-term mnemonic function (Lega et al, 2012; Watrous et al, 2013) in humans, but their specific role in long-term spatial memory function has remained unclear

Summary

| INTRODUCTION

Oscillations in the local field potential (LFP) reflect synchronous neural activity and are a likely candidate to integrate functional brain regions across multiple spatiotemporal scales (Fries et al, 2007; Buzsáki and Schomburg, 2015). PAC has been well documented in both human and animal studies during spatial (Tort et al, 2008; Lisman and Jensen, 2013; Newman et al, 2013; Bieri et al, 2014; Tamura et al, 2017), declarative (Fell et al, 2003; Tort et al, 2009; Axmacher et al, 2010; Lega et al, 2016), and sequence memory tasks (Heusser et al, 2016). Low and high gamma power peaked at different phases of low theta oscillations, consistent with animal studies (Colgin et al, 2009). These results support the hypothesis that theta-gamma PAC within the hippocampal formation contributes to successful longterm memory retrieval in humans

| METHODS

| RESULTS

Findings

| DISCUSSION