Elsevier

NeuroImage

Volume 66, 1 February 2013, Pages 642-647
NeuroImage

Successful memory encoding is associated with increased cross-frequency coupling between frontal theta and posterior gamma oscillations in human scalp-recorded EEG

https://doi.org/10.1016/j.neuroimage.2012.11.002Get rights and content

Abstract

Although previous studies have established that successful memory encoding is associated with increased synchronization of theta-band and gamma-band oscillations, it is unclear if there is a functional relationship between oscillations in these frequency bands. Using scalp-recorded EEG in healthy human participants, we demonstrate that cross-frequency coupling between frontal theta phase and posterior gamma power is enhanced during the encoding of visual stimuli which participants later on remember versus items which participants subsequently forget (“subsequent memory effect,” SME). Conventional wavelet analyses and source localizations revealed SMEs in spectral power of theta-, alpha-, and gamma-band. Successful compared to unsuccessful encoding was reflected in increased theta-band activity in right frontal cortex as well as increased gamma-band activity in parietal-occipital regions. Moreover, decreased alpha-band activity in prefrontal and occipital cortex was also related to successful encoding. Overall, these findings support the idea that during the formation of new memories frontal cortex regions interact with cortical representations in posterior areas.

Highlights

► Subsequent memory effects are reflected in theta-, alpha-, and gamma-band power. ► Coupling between theta and gamma oscillations increases during memory formation. ► Frontal theta oscillations might reflect involvement of a control system. ► Posterior gamma oscillations supposedly reflect activated cortical representations.

Introduction

Impressive evidence has been accumulated that synchronized neuronal activity serves the integration of spatially distributed processing in the brain ( Engel et al., 2001, Varela et al., 2001). In particular, oscillations in the gamma band range ( > 30 Hz) are thought to reflect processes related to the activation and maintenance of neuronal object representations ( Jensen et al., 2007 ). Low frequency oscillations in the theta band,~ 5 Hz, and in the alpha band, 8–12 Hz, have been related to top-down control modulating the processing of neuronal object representations ( Palva et al., 2005 ). Mostly based on animal research or studies with invasive recordings in epilepsy patients, several authors have suggested that the coordinated interplay of low- and high-frequency oscillations is likely to be crucial for various memory processes ( Canolty and Knight, 2010, Fell and Axmacher, 2011, Freunberger et al., 2011, Nyhus and Curran, 2010, Palva and Palva, 2007). So far, only a few studies using electroencephalography (EEG) or magnetencephalography (MEG) in humans have demonstrated cross-frequency coupling between low- and high-frequency oscillations in working memory and attention tasks ( Demiralp et al., 2007, Palva et al., 2005, Sauseng et al., 2008, Sauseng et al., 2009).

In the present study, we employed a subsequent memory paradigm to investigate whether low- and high-frequency oscillations in scalp-recorded EEG data interact during successful encoding of new memories. In a subsequent memory paradigm, neuronal activity during the encoding of stimuli which are remembered in a subsequent memory test, is contrasted versus activity during the encoding of stimuli which are later forgotten ( Paller and Wagner, 2002 ). Previous EEG/MEG studies on oscillatory brain activity have established “subsequent memory effects” (SME) in various frequency bands. Successful memory encoding has been found to be accompanied by increased synchrony in the theta and gamma band as well as by decreased synchrony in the alpha and beta band ( Gruber et al., 2004, Hanslmayr et al., 2009, Hanslmayr et al., 2011, Klimesch et al., 1996a, Klimesch et al., 1996b, Osipova et al., 2006). Most importantly, Osipova et al. (2006) found that increased frontal theta power coincided with enhanced gamma power in posterior cortex regions for later remembered versus later forgotten stimuli. The authors speculated that frontal theta oscillations might reflect top-down processes modulating gamma band activity related to neuronal representations in posterior regions. However, this hypothesis was not tested directly. On the basis of Osipova et al. (2006) , the main objectives of our study were (a) to confirm subsequent memory effects in theta, alpha, and gamma frequency bands, (b) to identify the cortical generators of these effects, and (c) to explore if posterior gamma power is coupled to the phases of frontal theta oscillations during the encoding of new information. This type of cross-frequency coupling would provide strong evidence for the notion that theta-oscillations play a pivotal role in long-range communication between brain regions involved in memory encoding processes.

Section snippets

Participants

A total of 26 healthy university students (23 female, M = 21.3 years, SD = 3.7) received either monetary compensation or course credits for participation. None of the participants reported any history of neurological or psychiatrical disorder. All participants had normal or corrected-to-normal vision. Informed consent was obtained from all participants according to the Declaration of Helsinki.

Stimuli and procedure

The stimuli consisted of 150 pictures of living (e.g. plants, animals) and 150 pictures of nonliving objects

Behavioral data

On average, 48.5% (SEM = 3.6%) of the encoding session items were remembered and 22.1% (SEM = 3.6%) were reported new. Counting remember responses to old items as hits and remember responses to new items as false alarms (M = 2.8, SEM = 1.0%), mean discrimination performance for remembered items was significantly larger than chance (d = 1.99; t22 = 17.2, p < .001).

SMEs in theta-, alpha-, and gamma-band power

Time-by-frequency representations of oscillatory activity are depicted in Fig. 1 as power changes relative to the 200 ms pre-stimulus baseline

Discussion

This study provides first strong evidence for a functional link between low- and high-frequency oscillations during the encoding of new memories. Phase-amplitude coupling between frontal theta oscillations and parietal gamma oscillations was found to be larger for subsequently remembered versus subsequently forgotten items. This coupling might reflect a mechanism by which theta-mediated control processes modulate gamma-band related processes implicated in the reactivation and maintenance of

Conclusion

Our study is the first to demonstrate increased cross-frequency coupling between EEG-recorded frontal theta and parietal/occipital gamma oscillations during the formation of new memories. Presumably, this coupling reflects interactions between a frontal control system and cortical representations activated and maintained in posterior brain regions.

Acknowledgments

This study was supported by grants to T.G. from the German Research Foundation (DFG). We are grateful to three anonymous reviewers for their constructive criticism.

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    These authors contributed equally to this work.

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