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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.
Highlights
Understanding the neural processes that mediate encoding of new memories is fundamental
Memory performance is shown by means of receiver operating characteristic (ROC) curves in Fig 1B and 1C, depicting memory performance in the MEG sample and the intracranial electroencephalography (iEEG) sample
The analyses described above demonstrate a functional dissociation of decreases in low-frequency and increases in higher-frequency power, suggesting that these changes do not reflect a Spectral fingerprints vs spectral tilt during memory formation single process
Summary
Understanding the neural processes that mediate encoding of new memories is fundamental. This change in the spectral pattern can result from two different processes: (1) a change in the “spectral tilt” (i.e., a shift from low-frequency activity to high-frequency activity [9,10,11]) or (2) changes at multiple distinct frequency bands related to distinct subprocesses involved in memory formation We contrast these two frameworks in a subsequent memory paradigm and show that memory-related frequency components can be dissociated on three levels: experimental condition, temporal dynamics, and brain regions. The “spectral fingerprints” framework arrives at very different predictions compared to the spectral “frequency tilt” framework It suggests that it should be possible to experimentally dissociate gamma power increases from theta and alpha/ beta power decreases. This combined measurement allowed us to capture changes in a large frequency range (2– 100 Hz) on a whole-brain and at a more local level
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