Maria Wimber

The Relationship between Brain Oscillations and BOLD Signal during Memory Formation: A Combined EEG–fMRI Study

Previous studies demonstrated that increases in the theta frequency band with concomitant decreases in the alpha/beta frequency band indicate successful memory formation. However, little is known about the brain regions and the cognitive processes that underlie these encoding-related oscillatory memory effects. We investigated this relationship using simultaneous EEG–fMRI recordings in humans during long-term memory encoding. In line with prior studies, we demonstrate that a decrease in beta power and an increase in theta power positively predict subsequent recall. In fMRI, stronger activity in the left inferior prefrontal cortex and the right parahippocampal gyrus correlated with successful memory formation. EEG source localization revealed that the subsequent memory effect in the beta band was localized in the left inferior prefrontal cortex, whereas the effect in the theta band was localized in medial temporal lobe regions. Trial-by-trial correlations between EEG and BOLD activity showed that beta power correlated negatively with left inferior prefrontal cortex activity. This correlation was more pronounced for items that could later be successfully recalled compared to items later forgotten. Based on these findings, we suggest that beta oscillations in the left inferior prefrontal cortex indicate semantic encoding processes, whereas theta oscillations in the medial temporal lobe reflect the binding of an item to its spatiotemporal context.

Retrieval from episodic memory: Neural mechanisms of interference resolution

Selectively retrieving a target memory among related memories requires some degree of inhibitory control over interfering and competing memories, a process assumed to be supported by inhibitory mechanisms. Evidence from behavioral studies suggests that such inhibitory control can lead to subsequent forgetting of the interfering information, a finding called retrieval-induced forgetting [Anderson, M. C., Bjork, R. A., & Bjork, E. L. Remembering can cause forgetting: Retrieval dynamics in long-term memory. Journal of Experimental Psychology: Learning, Memory & Cognition, 20, 1063–1087, 1994]. In the present functional magnetic resonance imaging study, we investigated the neural processes underlying retrieval-induced forgetting and, in particular, examined the extent to which these processes are retrieval (i.e., selection) specific. Participants actively retrieved a subset of previously studied material (selection condition), or were re-exposed to the same material for relearning (nonselection condition). Replicating prior behavioral work, selective retrieval caused significant forgetting of the nonretrieved items on a delayed recall test, relative to the re-exposure condition. Selective retrieval was associated with increased BOLD responses in the posterior temporal and parietal association cortices, in the bilateral hippocampus, and in the dorsolateral prefrontal cortex. Medial and lateral prefrontal areas showed a strong negative linear relationship between selection-related neural activity and subsequent forgetting of competitors. These findings suggest reduced demands on inhibitory control processes when interference is successfully resolved during early selective retrieval from episodic memory.

Neural Markers of Inhibition in Human Memory Retrieval

Retrieving particular information from memory facilitates the later retrieval of that information, but also impairs the later retrieval of related, interfering information. It has been theorized that this retrieval-induced forgetting reflects inhibition of interfering memory representations. We used event-related fMRI to investigate the functional neuroanatomy of this impaired retrieval, at the time the impairment is observed. Neural activity differences between impaired and facilitated information occurred in left ventrolateral prefrontal cortex (VLPFC, BA 45 and 47), precuneus (BA 7), and right inferior parietal lobule (IPL, BA 40). Activity in left anterior VLPFC (BA 47) and left posterior temporal cortex (BA 22), regions implicated in the controlled retrieval of weak semantic memory representations, predicted the degree of retrieval-induced forgetting. In contrast, activity in precuneus and right IPL predicted the degree of retrieval-induced facilitation. Our findings demonstrate that impairment of interfering memories and facilitation of practiced memories involve distinct neural processes, and suggest that the impairment reflects inhibition that weakens interfering memory representations.

Prestimulus Oscillatory Phase at 7 Hz Gates Cortical Information Flow and Visual Perception

Although we have the impression that visual information flows continuously from our sensory channels, recent studies indicate that this is likely not the case. Rather, we sample visual stimuli rhythmically, oscillating at 5-10 Hz. Electroencephalography (EEG) studies have demonstrated that this rhythmicity is reflected by the phase of ongoing brain oscillations in the same frequency. Theoretically, brain oscillations could underlie the rhythmic nature of perception by providing transient time windows for information exchange, but this question has not yet been systematically addressed. We recorded simultaneous EEG-fMRI while human participants performed a contour integration task and show that ongoing brain oscillations prior to stimulus onset predict functional connectivity between higher and lower level visual processing regions. Specifically, our results demonstrate that the phase of a 7 Hz oscillation prior to stimulus onset predicts perceptual performance and the bidirectional information flow between the left lateral occipital cortex and right intraparietal sulcus, as indicated by psychophysiological interaction and dynamic causal modeling. These findings suggest that human brain oscillations periodically gate visual perception at around 7 Hz by providing transient time windows for long-distance cortical information transfer. Such gating might be a general mechanism underlying the rhythmic nature of human perception.

The relationship between level of processing and hippocampal-cortical functional connectivity during episodic memory formation in humans

New episodic memory traces represent a record of the ongoing neocortical processing engaged during memory formation (encoding). Thus, during encoding, deep (semantic) processing typically establishes more distinctive and retrievable memory traces than does shallow (perceptual) processing, as assessed by later episodic memory tests. By contrast, the hippocampus appears to play a processing‐independent role in encoding, because hippocampal lesions impair encoding regardless of level of processing. Here, we clarified the neural relationship between processing and encoding by examining hippocampal–cortical connectivity during deep and shallow encoding. Participants studied words during functional magnetic resonance imaging and freely recalled these words after distraction. Deep study processing led to better recall than shallow study processing. For both levels of processing, successful encoding elicited activations of bilateral hippocampus and left prefrontal cortex, and increased functional connectivity between left hippocampus and bilateral medial prefrontal, cingulate and extrastriate cortices. Successful encoding during deep processing was additionally associated with increased functional connectivity between left hippocampus and bilateral ventrolateral prefrontal cortex and right temporoparietal junction. In the shallow encoding condition, on the other hand, pronounced functional connectivity increases were observed between the right hippocampus and the frontoparietal attention network activated during shallow study processing. Our results further specify how the hippocampus coordinates recording of ongoing neocortical activity into long‐term memory, and begin to provide a neural explanation for the typical advantage of deep over shallow study processing for later episodic memory. Hum Brain Mapp, 2013.

Prefrontal dopamine and the dynamic control of human long-term memory

Dopaminergic projections to the prefrontal cortex support higher-order cognitive functions, and are critically involved in many psychiatric disorders that involve memory deficits, including schizophrenia. The role of prefrontal dopamine in long-term memory, however, is still unclear. We used an imaging genetics approach to examine the hypothesis that dopamine availability in the prefrontal cortex selectively affects the ability to suppress interfering memories. Human participants were scanned via functional magnetic resonance imaging while practicing retrieval of previously studied target information in the face of interference from previously studied non-target information. This retrieval practice (RP) rendered the non-target information less retrievable on a later final test—a phenomenon known as retrieval-induced forgetting (RIF). In total, 54 participants were genotyped for the catechol-O-methyltransferase (COMT) Val108/158Met polymorphism. The COMT Val108/158Met genotype showed a selective and linear gene-dose effect on RIF, with the Met allele, which leads to higher prefrontal dopamine availability, being associated with greater RIF. Mirroring the behavioral pattern, the functional magnetic resonance imaging data revealed that Met allele carriers, compared with Val allele carriers, showed a greater response reduction in inhibitory control areas of the right inferior frontal cortex during RP, suggesting that they more efficiently reduced interference. These data support the hypothesis that the cortical dopaminergic system is centrally involved in the dynamic control of human long-term memory, supporting efficient remembering via the adaptive suppression of interfering memories.

Distinct Frontoparietal Networks Set the Stage for Later Perceptual Identification Priming and Episodic Recognition Memory

Recent imaging evidence suggests that a network of brain regions including the medial temporal lobe, ventrolateral prefrontal cortex, and dorsal posterior parietal cortex supports the successful encoding of long-term memories. Other areas, like the ventral posterior parietal and dorsolateral prefrontal cortices, have been associated with encoding failure rather than success. In line with the transfer-appropriate processing view, we hypothesized that distinct neural networks predict successful encoding depending on whether the later memory test draws primarily on perceptual or conceptual memory representations. Following an encoding phase, memory was assessed in a combined incidental perceptual identification and intentional recognition memory test. We found that during encoding, activation in ventral posterior parietal and dorsolateral prefrontal cortex predicted successful perceptual identification priming, whereas activation in ventrolateral prefrontal and dorsal posterior parietal cortex predicted successful recognition memory. Extending recent theories of attention to memory, the results suggest that ventral parietal regions support stimulus-driven attention to perceptual item features, forming memories accessed by later perceptual memory tests, whereas dorsal parietal regions support attention to meaningful item features, forming memories accessed by later conceptual memory tests.

Spurious correlations in simultaneous EEG-fMRI driven by in-scanner movement

Simultaneous EEG-fMRI provides an increasingly attractive research tool to investigate cognitive processes with high temporal and spatial resolution. However, artifacts in EEG data introduced by the MR scanner still remain a major obstacle. This study, employing commonly used artifact correction steps, shows that head motion, one overlooked major source of artifacts in EEG-fMRI data, can cause plausible EEG effects and EEG-BOLD correlations. Specifically, low-frequency EEG (<20Hz) is strongly correlated with in-scanner movement. Accordingly, minor head motion (<0.2mm) induces spurious effects in a twofold manner: Small differences in task-correlated motion elicit spurious low-frequency effects, and, as motion concurrently influences fMRI data, EEG-BOLD correlations closely match motion-fMRI correlations. We demonstrate these effects in a memory encoding experiment showing that obtained theta power (~3-7Hz) effects and channel-level theta-BOLD correlations reflect motion in the scanner. These findings highlight an important caveat that needs to be addressed by future EEG-fMRI studies.

Perceived time and temporal structure: Neural entrainment to isochronous stimulation increases duration estimates.

Distortions of perceived duration can give crucial insights into the mechanisms that underlie the processing and representation of stimulus timing. One factor that affects duration estimates is the temporal structure of stimuli that fill an interval. For example, regular filling (isochronous interval) leads to an overestimation of perceived duration as compared to irregular filling (anisochronous interval). In the present article, we use electroencephalography (EEG) to investigate the neural basis of this subjective lengthening of perceived duration with isochrony. In a two-interval forced choice task, participants judged which of two intervals lasts longer - one always being isochronous, the other one anisochronous. Response proportions confirm the subjective overestimation of isochronous intervals. At the neural level, isochronous sequences are associated with enhanced pairwise phase consistency (PPC) at the stimulation frequency, reflecting the brains entrainment to the regular stimulation. The PPC over the entrainment channels is further enhanced for isochronous intervals that are reported to be longer, and the magnitude of this PCC effect correlates with the amount of perceptual bias. Neural entrainment has been proposed as a mechanism of attentional selection, enabling increased neural responsiveness toward stimuli that arrive at an expected point in time. The present results support the proposed relationship between neural response magnitudes and temporal estimates: An increase in neural responsiveness leads to a more pronounced representation of the individual stimuli filling the interval and in turn to a subjective increase in duration.

Spatial mnemonic encoding: Theta power decreases and medial temporal lobe BOLD increases co-occur during the usage of the Method of Loci

Abstract 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.