Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation

Fellner, M.-C., Gollwitzer, S., Rampp, S., Kreiselmeyr, G., Bush, D., Diehl, B., Axmacher, N., Hamer, H. and Hanslmayr, S. (2019) Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation. PLoS Biology, 17(7), e3000403. (doi: 10.1371/journal.pbio.3000403) (PMID:31356598) (PMCID:PMC6687190)

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Abstract

Decreases in low-frequency power (2–30 Hz) alongside high-frequency power increases (>40 Hz) have been demonstrated to predict successful memory formation. Parsimoniously, this change in the frequency spectrum can be explained by one factor, a change in the tilt of the power spectrum (from steep to flat) indicating engaged brain regions. A competing view is that the change in the power spectrum contains several distinct brain oscillatory fingerprints, each serving different computations. Here, we contrast these two theories in a parallel magnetoencephalography (MEG)–intracranial electroencephalography (iEEG) study in which healthy participants and epilepsy patients, respectively, studied either familiar verbal material or unfamiliar faces. We investigated whether modulations in specific frequency bands can be dissociated in time and space and by experimental manipulation. Both MEG and iEEG data show that decreases in alpha/beta power specifically predicted the encoding of words but not faces, whereas increases in gamma power and decreases in theta power predicted memory formation irrespective of material. Critically, these different oscillatory signatures of memory encoding were evident in different brain regions. Moreover, high-frequency gamma power increases occurred significantly earlier compared to low-frequency theta power decreases. These results show that simple “spectral tilt” cannot explain common oscillatory changes and demonstrate that brain oscillations in different frequency bands serve different functions for memory encoding.

Item Type:Articles
Additional Information:This research was supported by grants from the Deutsche Forschungsgesellschaft (DFG; Emmy-Noether Programme; Nr. HA 5622/1-1; awarded to SH), the European Research Council (ERC Consolidator Grant Code4Memory Nr. 647954 awarded to SH), and the Economic and Social Sciences Research Council (TIME Nr. ES/R010072/1; awarded to SH) and funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)—Projektnummer 316803389—SFB 1280 (awarded to NA). SH is further supported by the Wolfson Society and Royal Society.
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Hanslmayr, Professor Simon
Creator Roles:
Hanslmayr, S.Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Writing – original draft, Writing – review and editing
Authors: Fellner, M.-C., Gollwitzer, S., Rampp, S., Kreiselmeyr, G., Bush, D., Diehl, B., Axmacher, N., Hamer, H., and Hanslmayr, S.
College/School:College of Medical Veterinary and Life Sciences > School of Psychology & Neuroscience
Journal Name:PLoS Biology
Publisher:Public Library of Science
ISSN:1544-9173
ISSN (Online):1545-7885
Copyright Holders:Copyright © 2019 Fellner et al.
First Published:First published in PLoS Biology 17(7): e3000403
Publisher Policy:Reproduced under a Creative Commons License

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