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 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.

Stress Elevates Frontal Midline Theta in Feedback-based Category Learning of Exceptions.

Adapting behavior based on category knowledge is a fundamental cognitive function, which can be achieved via different learning strategies relying on different systems in the brain. Whereas the learning of typical category members has been linked to implicit, prototype abstraction learning, which relies predominantly on prefrontal areas, the learning of exceptions is associated with explicit, exemplar-based learning, which has been linked to the hippocampus. Stress is known to foster implicit learning strategies at the expense of explicit learning. Procedural, prefrontal learning and cognitive control processes are reflected in frontal midline theta (4-8 Hz) oscillations during feedback processing. In the current study, we examined the effect of acute stress on feedback-based category learning of typical category members and exceptions and the oscillatory correlates of feedback processing in the EEG. A computational modeling procedure was applied to estimate the use of abstraction and exemplar strategies during category learning. We tested healthy, male participants who underwent either the socially evaluated cold pressor test or a nonstressful control procedure before they learned to categorize typical members and exceptions based on feedback. The groups did not differ significantly in their categorization accuracy or use of categorization strategies. In the EEG, however, stressed participants revealed elevated theta power specifically during the learning of exceptions, whereas the theta power during the learning of typical members did not differ between the groups. Elevated frontal theta power may reflect an increased involvement of medial prefrontal areas in the learning of exceptions under stress.

Brain oscillatory subsequent memory effects differ in power and long-range synchronization between semantic and survival processing.

Memory crucially depends on the way information is processed during encoding. Differences in processes during encoding not only lead to differences in memory performance but also rely on different brain networks. Although these assumptions are corroborated by several previous fMRI and ERP studies, little is known about how brain oscillations dissociate between different memory encoding tasks. The present study therefore compared encoding related brain oscillatory activity elicited by two very efficient encoding tasks: a typical deep semantic item feature judgment task and a more elaborative survival encoding task. Subjects were asked to judge words either for survival relevance or for animacy, as indicated by a cue presented prior to the item. This allowed dissociating pre-item activity from item-related activity for both tasks. Replicating prior studies, survival processing led to higher recognition performance than semantic processing. Successful encoding in the semantic condition was reflected by a strong decrease in alpha and beta power, whereas successful encoding in the survival condition was related to increased alpha and beta long-range phase synchrony. Moreover, a pre-item subsequent memory effect in theta power was found which did not vary with encoding condition. These results show that measures of local synchrony (power) and global long range-synchrony (phase synchronization) dissociate between memory encoding processes. Whereas semantic encoding was reflected in decreases in local synchrony, increases in global long range synchrony were related to elaborative survival encoding, presumably reflecting the involvement of a more widespread cortical network in this task.

The memory trace of a stressful episode.

Stress influences episodic memory formation via noradrenaline and glucocorticoid effects on amygdala and hippocampus. A common finding is the improvement of memory for central aspects of a stressful episode. This is putatively related to changes in the neural representations of specific experiences, i.e., their memory traces. Here we show that the memory improvement for objects that were encountered in a stressful episode relates to differences in the neural representations of these objects in the amygdala. Using functional magnetic resonance imaging, we found that stress specifically altered the representations of central objects: compared to control objects, they became more similar to one another and more distinct from objects that were not part of this episode. Furthermore, higher similarity of central objects to the main stressor-the faces of the stress-inducing committee members-predicted better memory. This suggests that the central objects were closely integrated into a stressor-centered memory representation. Our findings provide mechanistic insights into how stress shapes the memory trace and have profound implications for neurocognitive models of stressful and emotional memory.

Tracking Selective Rehearsal and Active Inhibition of Memory Traces in Directed Forgetting.

Selectively remembering or forgetting newly encountered information is essential for goal-directed behavior. It is still an open question, however, whether intentional forgetting is an active process based on the inhibition of unwanted memory traces or whether it occurs passively through reduced recruitment of selective rehearsal [1, 2]. Here, we show that intentional control of memory encoding relies on both, enhanced active inhibition and decreased selective rehearsal, and that these two processes can be separated in time and space. We applied representational similarity analysis (RSA [3]) and time-frequency analysis to EEG data during an item-method directed forgetting experiment [4]. We identified neural signatures of both, the intentional suppression and the voluntary upregulation of item-specific representations. Successful active forgetting was associated with a downregulation of item-specific representations in an early time window 500 ms after the instruction. This process was initiated by an increase in oscillatory alpha (8-13 Hz) power, a well-established signature of neural inhibition [5, 6], in occipital brain areas. During a later time window, 1500 ms after the cue, intentional forgetting was associated with reduced employment of active rehearsal processes, as reflected by an attenuated upregulation of item-specific representations as compared to intentionally encoded items. Our data show that active inhibition and selective rehearsal are two separate mechanisms whose consecutive employment allows for a voluntary control of memory formation.

Spatial Mnemonic Encoding: Theta Power Decreases and Medial Temporal Lobe BOLD Increases Co-Occur during the Usage of the Method of Loci.

The method of loci is one, if not the most, efficient mnemonic encoding strategy. This spatial mnemonic combines the core cognitive processes commonly linked to medial temporal lobe (MTL) activity: spatial and associative memory processes. During such processes, fMRI studies consistently demonstrate MTL activity, while electrophysiological studies have emphasized the important role of theta oscillations (3-8 Hz) in the MTL. However, it is still unknown whether increases or decreases in theta power co-occur with increased BOLD signal in the MTL during memory encoding. To investigate this question, we recorded EEG and fMRI separately, while human participants used the spatial method of loci or the pegword method, a similarly associative but nonspatial mnemonic. The more effective spatial mnemonic induced a pronounced theta power decrease source localized to the left MTL compared with the nonspatial associative mnemonic strategy. This effect was mirrored by BOLD signal increases in the MTL. Successful encoding, irrespective of the strategy used, elicited decreases in left temporal theta power and increases in MTL BOLD activity. This pattern of results suggests a negative relationship between theta power and BOLD signal changes in the MTL during memory encoding and spatial processing. The findings extend the well known negative relation of alpha/beta oscillations and BOLD signals in the cortex to theta oscillations in the MTL.

Entrainment of prefrontal beta oscillations induces an endogenous echo and impairs memory formation.

Brain oscillations across all frequency bands play a key role for memory formation. Specifically, desynchronization of local neuronal assemblies in the left inferior prefrontal cortex (PFC) in the beta frequency (∼18 Hz) has been shown to be central for encoding of verbal memories. However, it remains elusive whether prefrontal beta desynchronization is causally relevant for memory formation and whether these endogenous beta oscillations can be entrained by external stimulation. By using combined EEG-TMS (transcranial magnetic stimulation), we here address these fundamental questions in human participants performing a word-list learning task. Confirming our predictions, memory encoding was selectively impaired when the left inferior frontal gyrus (IFG) was driven at beta (18.7 Hz) compared to stimulation at other frequencies (6.8 Hz and 10.7 Hz) and to ineffective sham stimulation (18.7 Hz). Furthermore, a sustained oscillatory "echo" in the left IFG, which outlasted the stimulation period by approximately 1.5 s, was observed solely after beta stimulation. The strength of this beta echo was related to memory impairment on a between-subjects level. These results show endogenous oscillatory entrainment effects and behavioral impairment selectively in beta frequency for stimulation of the left IFG, demonstrating an intimate causal relationship between prefrontal beta desynchronization and memory formation.

Oscillatory power decreases and long-term memory: the information via desynchronization hypothesis.

The traditional belief is that brain oscillations are important for human long-term memory, because they induce synchronized firing between cell assemblies which shapes synaptic plasticity. Therefore, most prior studies focused on the role of synchronization for episodic memory, as reflected in theta (∼5 Hz) and gamma (>40 Hz) power increases. These studies, however, neglect the role that is played by neural desynchronization, which is usually reflected in power decreases in the alpha and beta frequency band (8-30 Hz). In this paper we present a first idea, derived from information theory that gives a mechanistic explanation of how neural desynchronization aids human memory encoding and retrieval. Thereby we will review current studies investigating the role of alpha and beta power decreases during long-term memory tasks and show that alpha and beta power decreases play an important and active role for human memory. Applying mathematical models of information theory, we demonstrate that neural desynchronization is positively related to the richness of information represented in the brain, thereby enabling encoding and retrieval of long-term memories. This information via desynchronization hypothesis makes several predictions, which can be tested in future experiments.