Staudigl, Tobias
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Across-subjects classification of stimulus modality from human MEG high frequency activity
Single-trial analyses have the potential to uncover meaningful brain dynamics that are obscured when averaging across trials. However, low signal-to-noise ratio (SNR) can impede the use of single-trial analyses and decoding methods. In this study, we investigate the applicability of a single-trial approach to decode stimulus modality from magnetoencephalographic (MEG) high frequency activity. In order to classify the auditory versus visual presentation of words, we combine beamformer source reconstruction with the random forest classification method. To enable group level inference, the classification is embedded in an across-subjects framework. We show that single-trial gamma SNR allows for good classification performance (accuracy across subjects: 66.44%). This implies that the characteristics of high frequency activity have a high consistency across trials and subjects. The random forest classifier assigned informational value to activity in both auditory and visual cortex with high spatial specificity. Across time, gamma power was most informative during stimulus presentation. Among all frequency bands, the 75 Hz to 95 Hz band was the most informative frequency band in visual as well as in auditory areas. Especially in visual areas, a broad range of gamma frequencies (55 Hz to 125 Hz) contributed to the successful classification. Thus, we demonstrate the feasibility of single-trial approaches for decoding the stimulus modality across subjects from high frequency activity and describe the discriminative gamma activity in time, frequency, and space.
Medial Prefrontal Theta Oscillations Track the Time Course of Interference during Selective Memory Retrieval
Memory retrieval is often challenged by other irrelevant competing memories that cause interference. This phenomenon is typically studied with the retrieval practice paradigm in which a category cue (e.g., Fruits) is presented together with an item-specific cue (e.g., Or::). Presentation of the category cue usually induces interference by reactivating competing memories (e.g., Banana, Apple, etc.), which is thought to be solved by means of inhibition, leading to retrieval-induced forgetting of these competing memories. Previous studies associated interference with an increase in medial prefrontal theta band (4–8 Hz) oscillations, but these studies could not disentangle the interference from the inhibition processes. We here used a retrieval practice procedure in which the category cue was presented before the item-specific cue to disentangle the interference from the inhibition signal. Furthermore, a competitive retrieval condition was contrasted with a noncompetitive condition. At a behavioral level, retrieval-induced forgetting was found in the competitive but not in the noncompetitive condition. At a neural level, presentation of the category cue elicited higher levels of theta power in the competitive condition, when compared with the noncompetitive retrieval condition. Importantly, this difference was localized to the ACC, which has been associated with the detection and mediation of interference. Additionally, theta power decreased upon presentation of the item-specific cue, and this difference was related to later forgetting. Our results therefore disentangle, for the first time, interference and inhibition in episodic memory retrieval and suggest that theta oscillations track the fine-grained temporal dynamics of interference during competitive memory retrieval.
Memory signals from the thalamus : Early thalamocortical phase synchronization entrains gamma oscillations during long-term memory retrieval
The thalamus is believed to be a key node in human memory networks, however, very little is known about its real-time functional role. Here we examined the dynamics of thalamocortical communication during long-term episodic memory retrieval in two experiments. In Experiment 1, intrathalamic and surface EEG was recorded in an epileptic patient implanted with depth electrodes for brain stimulation therapy. In a recognition memory test, early (300–500 ms) stimulus-linked oscillatory synchrony between mediodorsal thalamic and frontal surface electrodes at beta frequency (20 Hz) was enhanced for correctly remembered old compared to correctly rejected new items. Directionality measures (Granger causality) indicated that the thalamus was the sender, and the neocortex the receiver, of this beta signal, which also modulated the power of neocortical gamma (55–80 Hz) oscillations (cross-frequency coupling). Experiment 2 validated the cross-frequency coupling effects in a healthy participant sample. Confirming the findings from Experiment 1, significantly increased cross-frequency coupling was found over frontal scalp electrodes during successful recognition. Extending anatomical knowledge on thalamic connectivity with frontal neocortex, these results suggest that the thalamus sends an early memory signal to frontal regions, triggering further memory search processes.
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.
No Evidence for Memory Decontextualization across One Night of Sleep
Sleep after learning strengthens memory consolidation. According to the active system consolidation hypothesis, sleep supports the integration of newly acquired memories into cortical knowledge networks, presumably accompanied by a process of decontextualization of the memory trace (i.e., a gradual loss of memory for the learning context). However, the availability of contextual information generally facilitates memory recall and studies on the interaction of sleep and context on memory retrieval have revealed inconsistent results. Here, we do not find any evidence for a role of sleep in the decontextualization of newly learned declarative memories. In two separate studies, 104 healthy young adults incidentally learned words associated with a context. After a 12 h retention interval filled with either sleep or wakefulness, recall (Experiment 1) or recognition (Experiment 2) was tested with the same or different context. Overall, memory retrieval was significantly improved when the learning context was reinstated, as compared to a different context. However, this context effect of memory was not modulated by sleep vs. wakefulness. These findings argue against a decontextualization of memories, at least across a single night of sleep.
How brain oscillations form memories : a processing based perspective on oscillatory subsequent memory effects
Brain oscillations are increasingly recognized by memory researchers as a useful tool to unravel the neural mechanisms underlying the formation of a memory trace. However, the increasing numbers of published studies paint a rather complex picture of the relation between brain oscillations and memory formation. Concerning oscillatory amplitude, for instance, increases as well as decreases in various frequency bands (theta, alpha, beta and gamma) were associated with memory formation. These results cast doubt on frameworks putting forward the idea of an oscillatory signature that is uniquely related to memory formation. In an attempt to clarify this issue we here provide an alternative perspective, derived from classic cognitive frameworks/principles of memory. On the basis of Craik's levels of processing framework and Tulving's encoding specificity principle we hypothesize that brain oscillations during encoding might primarily reflect the perceptual and cognitive processes engaged by the encoding task. These processes may then lead to later successful retrieval depending on their overlap with the processes engaged by the memory test. As a consequence, brain oscillatory correlates of memory formation could vary dramatically depending on how the memory is encoded, and on how it is being tested later. Focusing on oscillatory amplitude changes and on theta-to-gamma cross-frequency coupling, we here review recent evidence showing how brain oscillatory subsequent memory effects can be modulated, and sometimes even be reversed, by varying encoding tasks, and the contextual overlap between encoding and retrieval.
Prefrontally Driven Downregulation of Neural Synchrony Mediates Goal-Directed Forgetting
Neural synchronization between distant cell assemblies is crucial for the formation of new memories. To date, however, it remains unclear whether higher-order brain regions can adaptively regulate neural synchrony to control memory processing in humans. We explored this question in two experiments using a voluntary forgetting task. In the first experiment, we simultaneously recorded electroencephalography along with fMRI. The results show that a reduction in neural synchrony goes hand-in-hand with a BOLD signal increase in the left dorsolateral prefrontal cortex (dlPFC) when participants are cued to forget previously studied information. In the
second experiment, we directly stimulated the left dlPFC with repetitive transcranial magnetic stimulation during the same task, and show that such stimulation specifically boosts the behavioral forgetting effect and induces a reduction in neural synchrony. These results suggest that prefrontally driven downregulation of long-range neural synchronization mediates goal-directed forgetting of long-term memories.
Temporal-Pattern Similarity Analysis Reveals the Beneficial and Detrimental Effects of Context Reinstatement on Human Memory
A powerful force in human memory is the context in which memories are encoded (Tulving and Thomson, 1973). Several studies suggest that the reinstatement of neural encoding patterns is beneficial for memory retrieval (Manning et al., 2011; Staresina et al., 2012; Jafarpour et al., 2014). However, reinstatement of the original encoding context is not always helpful, for instance, when retrieving a memory in a different contextual situation (Smith and Vela, 2001). It is an open question whether such context-dependent memory effects can be captured by the reinstatement of neural patterns. We investigated this question by applying temporal and spatial pattern similarity analysis in MEG and intracranial EEG in a context-match paradigm. Items (words) were tagged by individual dynamic context stimuli (movies). The results show that beta oscillatory phase in visual regions and the parahippocampal cortex tracks the incidental reinstatement of individual context trajectories on a single-trial level. Crucially, memory benefitted from reinstatement when the encoding and retrieval contexts matched but suffered from reinstatement when the contexts did not match.
Theta Oscillations at Encoding Mediate the Context-Dependent Nature of Human Episodic Memory
Human episodic memory is highly context dependent. Therefore, retrieval benefits when a memory is recalled in the same context compared to a different context. This implies that items and contexts are bound together during encoding, such that the reinstatement of the initial context at test improves retrieval. Animal studies suggest that theta oscillations and theta-to-gamma cross-frequency coupling modulate such item-context binding, but direct evidence from humans is scarce. We investigated this issue by manipulating the overlap of contextual features between encoding and retrieval. Participants studied words superimposed on movie clips and were later tested by presenting the word with either the same or a different movie. The results show that memory performance and the oscillatory correlates of memory formation crucially depend on the overlap of the context between encoding and test. When the context matched, high theta power during encoding was related to successful recognition, whereas the opposite pattern emerged in the context-mismatch condition. In addition, cross-frequency coupling analysis revealed a context-dependent theta-to-gamma memory effect specifically in the left hippocampus. These results reveal for the first time that context-dependent episodic memory effects are mediated by theta oscillatory activity.
Rapid memory reactivation revealed by oscillatory entrainment.
Episodic memory refers to humans' unique ability to mentally reconstruct past events. Neurocomputational models predict that remembering entails the reinstatement of brain activity that was present when an event was initially experienced [ [1], [2], [3], [4] and [5]], a claim that has recently gained support from functional imaging work in humans [ [6], [7], [8], [9], [10], [11], [12], [13] and [14]]. The nature of this reactivation, however, is still unclear. Cognitive models claim that retrieval is set off by an early reactivation of stored memory representations (“ecphory”) [ [15], [16] and [17]]. However, reinstatement as found in imaging studies might also reflect postretrieval processes that operate on the products of retrieval and are thus a consequence rather than a precondition of remembering. Here, we used frequency entrainment as a novel method of tagging memories in the human electroencephalogram (EEG). Participants studied words presented on flickering backgrounds, entraining a steady-state brain response at either 6 or 10 Hz. We found that these frequency signatures rapidly reemerged during a later memory test when participants successfully recognized a word. An additional behavioral experiment suggested that this reactivation occurs in the absence of conscious memory for the frequencies entrained during study. The findings provide empirical evidence for the role of rapid, likely unconscious memory reactivation during retrieval.