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

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  • Marie-Christin Fellner
  • Stephanie Gollwitzer
  • Stefan Rampp
  • Gernot Kreiselmeyr
  • Daniel Bush
  • Beate Diehl
  • Nikolai Axmacher
  • Hajo Hamer
  • Simon Hanslmayr

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.There are two competing explanations for electrophysiological signatures during cognitive processes. One assumes simultaneous increases in high frequencies paired with decreases in low frequencies, whereas the other suggests that different frequencies index separate oscillatory processes. This study reports data that support the latter view.

Suggested Citation

  • Marie-Christin Fellner & Stephanie Gollwitzer & Stefan Rampp & Gernot Kreiselmeyr & Daniel Bush & Beate Diehl & Nikolai Axmacher & Hajo Hamer & Simon Hanslmayr, 2019. "Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation," PLOS Biology, Public Library of Science, vol. 17(7), pages 1-30, July.
  • Handle: RePEc:plo:pbio00:3000403
    DOI: 10.1371/journal.pbio.3000403
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    References listed on IDEAS

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    1. Anne Keitel & Joachim Gross, 2016. "Individual Human Brain Areas Can Be Identified from Their Characteristic Spectral Activation Fingerprints," PLOS Biology, Public Library of Science, vol. 14(6), pages 1-22, June.
    2. E. A. Solomon & J. E. Kragel & M. R. Sperling & A. Sharan & G. Worrell & M. Kucewicz & C. S. Inman & B. Lega & K. A. Davis & J. M. Stein & B. C. Jobst & K. A. Zaghloul & S. A. Sheth & D. S. Rizzuto & , 2017. "Widespread theta synchrony and high-frequency desynchronization underlies enhanced cognition," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    3. Sebastian Michelmann & Bernhard P. Staresina & Howard Bowman & Simon Hanslmayr, 2019. "Speed of time-compressed forward replay flexibly changes in human episodic memory," Nature Human Behaviour, Nature, vol. 3(2), pages 143-154, February.
    4. Kai J Miller & Gerwin Schalk & Dora Hermes & Jeffrey G Ojemann & Rajesh P N Rao, 2016. "Spontaneous Decoding of the Timing and Content of Human Object Perception from Cortical Surface Recordings Reveals Complementary Information in the Event-Related Potential and Broadband Spectral Chang," PLOS Computational Biology, Public Library of Science, vol. 12(1), pages 1-20, January.
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