Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Fellner, Marie-Christin, Gollwitzer, Stephanie, Rampp, Stefan, Kreiselmeyr, Gernot, Bush, Daniel, Diehl, Beate, Axmacher, Nikolai, Hamer, Hajo, Hanslmayr, Simon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687190/
https://www.ncbi.nlm.nih.gov/pubmed/31356598
http://dx.doi.org/10.1371/journal.pbio.3000403
_version_ 1783442696623357952
author Fellner, Marie-Christin
Gollwitzer, Stephanie
Rampp, Stefan
Kreiselmeyr, Gernot
Bush, Daniel
Diehl, Beate
Axmacher, Nikolai
Hamer, Hajo
Hanslmayr, Simon
author_facet Fellner, Marie-Christin
Gollwitzer, Stephanie
Rampp, Stefan
Kreiselmeyr, Gernot
Bush, Daniel
Diehl, Beate
Axmacher, Nikolai
Hamer, Hajo
Hanslmayr, Simon
author_sort Fellner, Marie-Christin
collection PubMed
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.
format Online
Article
Text
id pubmed-6687190
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-66871902019-08-15 Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation Fellner, Marie-Christin Gollwitzer, Stephanie Rampp, Stefan Kreiselmeyr, Gernot Bush, Daniel Diehl, Beate Axmacher, Nikolai Hamer, Hajo Hanslmayr, Simon PLoS Biol Research Article 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. Public Library of Science 2019-07-29 /pmc/articles/PMC6687190/ /pubmed/31356598 http://dx.doi.org/10.1371/journal.pbio.3000403 Text en © 2019 Fellner et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Fellner, Marie-Christin
Gollwitzer, Stephanie
Rampp, Stefan
Kreiselmeyr, Gernot
Bush, Daniel
Diehl, Beate
Axmacher, Nikolai
Hamer, Hajo
Hanslmayr, Simon
Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation
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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6687190/
https://www.ncbi.nlm.nih.gov/pubmed/31356598
http://dx.doi.org/10.1371/journal.pbio.3000403
work_keys_str_mv AT fellnermariechristin spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT gollwitzerstephanie spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT ramppstefan spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT kreiselmeyrgernot spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT bushdaniel spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT diehlbeate spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT axmachernikolai spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT hamerhajo spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation
AT hanslmayrsimon spectralfingerprintsorspectraltiltevidencefordistinctoscillatorysignaturesofmemoryformation