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

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 MEG-intracranial EEG study where 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, 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 speak against a "spectral tilt" and demonstrate that brain oscillations in different frequency bands serve different functions for memory encoding.

Fluctuations in functional connectivity associated with interictal epileptiform discharges (IEDs) in intracranial EEG

“…While these interactions can be spurious and require strict testing for the presence of oscillations above the 1/f background and against null models that preserve autocorrelation[56, 57], a detailed investigation of which of these interactions are changed during IEDs would help further elucidate the neurophysiological processes that they disrupt. Second, opposing changes in high- and low-frequency bands can sometimes be explained by changes in the slope of the 1/f background, rather than changes in each band individually[58]. In studies of neural activation, the slope and power in specific bands are directly and intuitively related, however it is unclear if such a relationship exists for connectivity.…”

Theta power and theta‐gamma coupling support long‐term spatial memory retrieval

“…Other studies performing a different hybrid navigation and memory paradigm have suggested diverse roles for low theta depending on laterality and hippocampal subregion (Miller et al, 2018;Goyal et al, 2020;Herweg et al, 2020). There has been an increasing body of evidence to suggest that low frequency power decrease and high frequency power increase is associated with performance in a variety of tasks, with this "tilt" in the 1/frequency characteristic inherent to human EEG thought to reflect increased regional neural activity (Fellner et al, 2019). However, we found that low and high theta power increases alone after correction for multiple comparisons were associated with task performance, as previously reported in both MEG (Kaplan et al, 2012) and intracranial EEG (Miller et al, 2018) studies.…”

Hippocampal theta codes for distances in semantic and temporal spaces

“…Although a useful paradigm, the SME is not a direct test that theta specifically supports the formation or retrieval of associations between items in memory, i.e., a cognitive map of recently acquired information. Moreover, many similar studies report the opposite effect: a hippocampal or cortical decrease in theta power during successful encoding or retrieval (33)(34)(35)(36)(37)(38). These conflicting findings raise serious questions about whether the neural processing of spatial and episodic information relies on the same theta-based mechanisms.…”