Erik A. Wing

Neural Similarity Between Encoding and Retrieval is Related to Memory Via Hippocampal Interactions

A fundamental principle in memory research is that memory is a function of the similarity between encoding and retrieval operations. Consistent with this principle, many neurobiological models of declarative memory assume that memory traces are stored in cortical regions, and the hippocampus facilitates the reactivation of these traces during retrieval. The present investigation tested the novel prediction that encoding-retrieval similarity can be observed and related to memory at the level of individual items. Multivariate representational similarity analysis was applied to functional magnetic resonance imaging data collected during encoding and retrieval of emotional and neutral scenes. Memory success tracked fluctuations in encoding-retrieval similarity across frontal and posterior cortices. Importantly, memory effects in posterior regions reflected increased similarity between item-specific representations during successful recognition. Mediation analyses revealed that the hippocampus mediated the link between cortical similarity and memory success, providing crucial evidence for hippocampal-cortical interactions during retrieval. Finally, because emotional arousal is known to modulate both perceptual and memory processes, similarity effects were compared for emotional and neutral scenes. Emotional arousal was associated with enhanced similarity between encoding and retrieval patterns. These findings speak to the promise of pattern similarity measures for evaluating memory representations and hippocampal-cortical interactions.

Reinstatement of individual past events revealed by the similarity of distributed activation patterns during encoding and retrieval

Neurobiological memory models assume memory traces are stored in neocortex, with pointers in the hippocampus, and are then reactivated during retrieval, yielding the experience of remembering. Whereas most prior neuroimaging studies on reactivation have focused on the reactivation of sets or categories of items, the current study sought to identify cortical patterns pertaining to memory for individual scenes. During encoding, participants viewed pictures of scenes paired with matching labels (e.g., “barn,” “tunnel”), and, during retrieval, they recalled the scenes in response to the labels and rated the quality of their visual memories. Using representational similarity analyses, we interrogated the similarity between activation patterns during encoding and retrieval both at the item level (individual scenes) and the set level (all scenes). The study yielded four main findings. First, in occipitotemporal cortex, memory success increased with encoding-retrieval similarity (ERS) at the item level but not at the set level, indicating the reactivation of individual scenes. Second, in ventrolateral pFC, memory increased with ERS for both item and set levels, indicating the recapitulation of memory processes that benefit encoding and retrieval of all scenes. Third, in retrosplenial/posterior cingulate cortex, ERS was sensitive to individual scene information irrespective of memory success, suggesting automatic activation of scene contexts. Finally, consistent with neurobiological models, hippocampal activity during encoding predicted the subsequent reactivation of individual items. These findings show the promise of studying memory with greater specificity by isolating individual mnemonic representations and determining their relationship to factors like the detail with which past events are remembered.

The neural basis of involuntary episodic memories

Voluntary episodic memories require an intentional memory search, whereas involuntary episodic memories come to mind spontaneously without conscious effort. Cognitive neuroscience has largely focused on voluntary memory, leaving the neural mechanisms of involuntary memory largely unknown. We hypothesized that, because the main difference between voluntary and involuntary memory is the controlled retrieval processes required by the former, there would be greater frontal activity for voluntary than involuntary memories. Conversely, we predicted that other components of the episodic retrieval network would be similarly engaged in the two types of memory. During encoding, all participants heard sounds, half paired with pictures of complex scenes and half presented alone. During retrieval, paired and unpaired sounds were presented, panned to the left or to the right. Participants in the involuntary group were instructed to indicate the spatial location of the sound, whereas participants in the voluntary group were asked to additionally recall the pictures that had been paired with the sounds. All participants reported the incidence of their memories in a postscan session. Consistent with our predictions, voluntary memories elicited greater activity in dorsal frontal regions than involuntary memories, whereas other components of the retrieval network, including medial-temporal, ventral occipitotemporal, and ventral parietal regions were similarly engaged by both types of memories. These results clarify the distinct role of dorsal frontal and ventral occipitotemporal regions in predicting strategic retrieval and recalled information, respectively, and suggest that, although there are neural differences in retrieval, involuntary memories share neural components with established voluntary memory systems.

Neural correlates of retrieval-based memory enhancement: An fMRI study of the testing effect

Restudying material is a common method for learning new information, but not necessarily an effective one. Research on the testing effect shows that practice involving retrieval from memory can facilitate later memory in contrast to passive restudy. Despite extensive behavioral work, the brain processes that make retrieval an effective learning strategy remain unclear. In the present experiment, we explored how initially retrieving items affected memory a day later as compared to a condition involving traditional restudy. In contrast to restudy, initial testing that contributed to future memory success was associated with engagement of several regions including the anterior hippocampus, lateral temporal cortices, and medial prefrontal cortex (PFC). Additionally, testing enhanced hippocampal connectivity with ventrolateral PFC and midline regions. These findings indicate that the testing effect may be contingent on processes that are typically thought to support memory success at encoding (e.g. relational binding, selection and elaboration of semantically-related information) in addition to those more often associated with retrieval (e.g. memory search).

Hippocampal Contributions to the Large-Scale Episodic Memory Network Predict Vivid Visual Memories

Abstract A common approach in memory research is to isolate the function(s) of individual brain regions, such as the hippocampus, without addressing how those regions interact with the larger network. To investigate the properties of the hippocampus embedded within large‐scale networks, we used functional magnetic resonance imaging and graph theory to characterize complex hippocampal interactions during the active retrieval of vivid versus dim visual memories. The study yielded 4 main findings. First, the right hippocampus displayed greater communication efficiency with the network (shorter path length) and became a more convergent structure for information integration (higher centrality measures) for vivid than dim memories. Second, vivid minus dim differences in our graph theory measures of interest were greater in magnitude for the right hippocampus than for any other region in the 90‐region network. Moreover, the right hippocampus significantly reorganized its set of direct connections from dim to vivid memory retrieval. Finally, beyond the hippocampus, communication throughout the whole‐brain network was more efficient (shorter global path length) for vivid than dim memories. In sum, our findings illustrate how multivariate network analyses can be used to investigate the roles of specific regions within the large‐scale network, while also accounting for global network changes.

On known unknowns: Fluency and the neural mechanisms of illusory truth

The “illusory truth” effect refers to the phenomenon whereby repetition of a statement increases its likelihood of being judged true. This phenomenon has important implications for how we come to believe oft-repeated information that may be misleading or unknown. Behavioral evidence indicates that fluency, the subjective ease experienced while processing information, underlies this effect. This suggests that illusory truth should be mediated by brain regions previously linked to fluency, such as the perirhinal cortex (PRC). To investigate this possibility, we scanned participants with fMRI while they rated the truth of unknown statements, half of which were presented earlier (i.e., repeated). The only brain region that showed an interaction between repetition and ratings of perceived truth was PRC, where activity increased with truth ratings for repeated, but not for new, statements. This finding supports the hypothesis that illusory truth is mediated by a fluency mechanism and further strengthens the link between PRC and fluency.

Search and recovery of autobiographical and laboratory memories: Shared and distinct neural components

ABSTRACT Functional neuroimaging evidence suggests that there are differences in the neural correlates of episodic memory for laboratory stimuli (laboratory memory) and for events from ones own life (autobiographical memory). However, this evidence is scarce and often confounded with differences in memory testing procedures. Here, we directly compared the neural mechanisms underlying the search and recovery of autobiographical and laboratory memories while minimizing testing differences. Before scanning, participants completed a laboratory memory encoding task in which they studied four‐word “chains” spread across three word pairs. During scanning, participants completed a laboratory memory retrieval task, in which they recalled the word chains, and an autobiographical memory retrieval task, in which they recalled specific personal events associated with word cues. Importantly, response times were similar in the two tasks, allowing for a direct comparison of the activation time courses. We found that during memory search (searching for the memory target), similar brain regions were activated during both the autobiographical and laboratory tasks, whereas during memory recovery (accessing the memory traces; i.e., ecphory), clear differences emerged: regions of the default mode network (DMN) were activated greater during autobiographical than laboratory memory, whereas the bilateral superior parietal lobules were activated greater during laboratory than autobiographical memory. Also, multivariate functional connectivity analyses revealed that regardless of memory stage, the DMN and ventral attention network exhibited a more integrated topology in the functional network underlying autobiographical (vs. laboratory) memory retrieval, whereas the fronto‐parietal task control network exhibited a more integrated topology in the functional network underlying laboratory (vs. autobiographical) memory retrieval. These findings further characterize the shared and distinct neural components underlying autobiographical and laboratory memories, and suggest that differences in autobiographical vs. laboratory memory brain activation previously reported in the literature reflect memory recovery rather than search differences. Graphical abstract Figure. No caption available. HighlightsWe compared autobiographical (AM) vs. laboratory (LM) memory retrieval.Task brain activation differences occurred during memory recovery but not search.The default mode network was more strongly activated during AM recovery.The superior parietal lobules were more strongly activated during LM recovery.The default mode network exhibited a more integrated topology during AM.

Neural mechanisms underlying subsequent memory for personal beliefs:An fMRI study

Many fMRI studies have examined the neural mechanisms supporting emotional memory for stimuli that generate emotion rather automatically (e.g., a picture of a dangerous animal or of appetizing food). However, far fewer studies have examined how memory is influenced by emotion related to social and political issues (e.g., a proposal for large changes in taxation policy), which clearly vary across individuals. In order to investigate the neural substrates of affective and mnemonic processes associated with personal opinions, we employed an fMRI task wherein participants rated the intensity of agreement/disagreement to sociopolitical belief statements paired with neural face pictures. Following the rating phase, participants performed an associative recognition test in which they distinguished identical versus recombined face–statement pairs. The study yielded three main findings: behaviorally, the intensity of agreement ratings was linked to greater subjective emotional arousal as well as enhanced high-confidence subsequent memory. Neurally, statements that elicited strong (vs. weak) agreement or disagreement were associated with greater activation of the amygdala. Finally, a subsequent memory analysis showed that the behavioral memory advantage for statements generating stronger ratings was dependent on the medial prefrontal cortex (mPFC). Together, these results both underscore consistencies in neural systems supporting emotional arousal and suggest a modulation of arousal-related encoding mechanisms when emotion is contingent on referencing personal beliefs.

Excitatory TMS Boosts Memory Representations

Brain stimulation technologies have seen increasing application in basic science investigations, specifically towards the goal of improving memory functioning. However, proposals concerning the neural mechanisms underlying cognitive enhancement often rely on simplified notions of excitation and, most applications examining the effects of transcranial magnetic stimulation (TMS) on functional neuroimaging measures have been limited to univariate analyses of brain activity. We present here analyses using representational similarity analysis (RSA) and encoding-retrieval similarity (ERS) analysis in order to quantify the effect of TMS on memory representations. To test whether an increase in local excitability in PFC can have measurable influences on upstream representations in earlier temporal memory regions, we compared 1Hz and 5Hz stimulation to the left dorsolateral PFC. We found that 10 minutes of 5Hz rTMS, relative to 1Hz, had multiple effects on neural representations: 1) greater RSA during both encoding and retrieval, 2) greater ERS across all items, and, critically, 3) increasing ERS in MTL with increasing univariate activity in DLPFC, and greater functional connectivity for hits than misses between these regions. These results provide the first evidence of rTMS enhancing semantic representations and strengthen the idea that rTMS may affect the reinstatement of previously experienced events in upstream regions.

Contributions of the ventral parietal cortex to declarative memory

Our understanding of the role that ventral parietal cortex (VPC) plays in declarative memory processes has changed dramatically over the last two decades. The goal of this chapter is to provide a concise overview data concerning VPC involvement in episodic memory (EM), and to connect this data to several key theories of VPC function. We review evidence from five methodological domains in cognitive neuroscience: neuropsychological lesion evidence, univariate activation studies, multivoxel pattern analyses, functional connectivity studies, and brain stimulation experiments. We discuss how the body of empirical work bears on putative mnemonic functions of VPC related to attention and stimulus representation, and detail the strengths and weaknesses of related theories. Lastly, we identify several broad conceptual questions raised by recent investigations, and outline directions for future research.