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

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...

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Main Authors: Marie-Christin Fellner, Stephanie Gollwitzer, Stefan Rampp, Gernot Kreiselmeyr, Daniel Bush, Beate Diehl, Nikolai Axmacher, Hajo Hamer, Simon Hanslmayr
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-07-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3000403
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author Marie-Christin Fellner
Stephanie Gollwitzer
Stefan Rampp
Gernot Kreiselmeyr
Daniel Bush
Beate Diehl
Nikolai Axmacher
Hajo Hamer
Simon Hanslmayr
author_facet Marie-Christin Fellner
Stephanie Gollwitzer
Stefan Rampp
Gernot Kreiselmeyr
Daniel Bush
Beate Diehl
Nikolai Axmacher
Hajo Hamer
Simon Hanslmayr
author_sort Marie-Christin Fellner
collection DOAJ
description 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.
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spelling doaj.art-f1f2fd0ae25f41f1b752a10299f570f32022-12-21T19:12:37ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852019-07-01177e300040310.1371/journal.pbio.3000403Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.Marie-Christin FellnerStephanie GollwitzerStefan RamppGernot KreiselmeyrDaniel BushBeate DiehlNikolai AxmacherHajo HamerSimon HanslmayrDecreases 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.https://doi.org/10.1371/journal.pbio.3000403
spellingShingle Marie-Christin Fellner
Stephanie Gollwitzer
Stefan Rampp
Gernot Kreiselmeyr
Daniel Bush
Beate Diehl
Nikolai Axmacher
Hajo Hamer
Simon Hanslmayr
Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.
PLoS Biology
title Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.
title_full Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.
title_fullStr Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.
title_full_unstemmed Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.
title_short Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation.
title_sort spectral fingerprints or spectral tilt evidence for distinct oscillatory signatures of memory formation
url https://doi.org/10.1371/journal.pbio.3000403
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