Content representation in the human medial temporal lobe

The transformation of sensory inputs into complex memory representations is fundamental to human experience; yet, little is known about how this crucial process is achieved. When you meet your friend at the new cafe in town, what part of the brain encodes this novel scene into long term memory? What part encoded your friend’s favorite t-shirt, so that the sight of it gives you a feeling of familiarity rather than surprise? It is well-established that the medial temporal lobe (MTL) is crucial to both processes, but the MTL is not a single homogeneous region. In fact, it is composed of several anatomically distinct subregions including hippocampus, perirhinal cortex (PRC) and parahippocampal cortex (PHC). However, the computations performed by each subregion to encode individual events is still unclear. The present research tests the central hypothesis that different forms of event content are transformed into memory by distinct subregions within the MTL. A critical barrier in the study of content representation thus far has been its focus on comparing univariate peak activations in a region to different stimulus materials. To go beyond this limited approach, we employed multivariate statistical analyses that takes into account how event content is represented by distributed activity in MTL subregions. First, we examine the content-specific contributions of MTL subregions to episodic encoding and retrieval. Then, we demonstrate how these distributed representations support memory-based prediction to resolve ambiguities in our environment.Neuroscienc

Consolidation of complex events via reinstatement in posterior cingulate cortex

It is well-established that active rehearsal increases the efficacy of memory consolidation. It is also known that complex events are interpreted with reference to prior knowledge. However, comparatively little attention has been given to the neural underpinnings of these effects. In healthy adult humans, we investigated the impact of effortful, active rehearsal on memory for events by showing people several short video clips and then asking them to recall these clips, either aloud (Experiment 1) or silently while in an MRI scanner (Experiment 2). In both experiments, actively rehearsed clips were remembered in far greater detail than unrehearsed clips when tested a week later. In Experiment 1, highly similar descriptions of events were produced across retrieval trials, suggesting a degree of semanticization of the memories had taken place. In Experiment 2, spatial patterns of BOLD signal in medial temporal and posterior midline regions were correlated when encoding and rehearsing the same video. Moreover, the strength of this correlation in the posterior cingulate predicted the amount of information subsequently recalled. This is likely to reflect a strengthening of the representation of the video's content. We argue that these representations combine both new episodic information and stored semantic knowledge (or "schemas"). We therefore suggest that posterior midline structures aid consolidation by reinstating and strengthening the associations between episodic details and more generic schematic information. This leads to the creation of coherent memory representations of lifelike, complex events that are resistant to forgetting, but somewhat inflexible and semantic-like in nature

Neural similarity between overlapping events at learning differentially affects reinstatement across the cortex

Episodic memory often involves high overlap between the actors, locations, and objects of everyday events. Under some circumstances, it may be beneficial to distinguish, or differentiate, neural representations of similar events to avoid interference at recall. Alternatively, forming overlapping representations of similar events, or integration, may aid recall by linking shared information between memories. It is currently unclear how the brain supports these seemingly conflicting functions of differentiation and integration. We used multivoxel pattern similarity analysis (MVPA) of fMRI data and neural-network analysis of visual similarity to examine how highly overlapping naturalistic events are encoded in patterns of cortical activity, and how the degree of differentiation versus integration at encoding affects later retrieval. Participants performed an episodic memory task in which they learned and recalled naturalistic video stimuli with high feature overlap. Visually similar videos were encoded in overlapping patterns of neural activity in temporal, parietal, and occipital regions, suggesting integration. We further found that encoding processes differentially predicted later reinstatement across the cortex. In visual processing regions in occipital cortex, greater differentiation at encoding predicted later reinstatement. Higher-level sensory processing regions in temporal and parietal lobes showed the opposite pattern, whereby highly integrated stimuli showed greater reinstatement. Moreover, integration in high-level sensory processing regions during encoding predicted greater accuracy and vividness at recall. These findings provide novel evidence that encoding-related differentiation and integration processes across the cortex have divergent effects on later recall of highly similar naturalistic events

Reinstatement of memory representations for lifelike events over the course of a week

When we remember an event, the content of that memory is represented across the brain. Detailed memory retrieval is thought to involve the reinstatement of those representations. Functional MRI combined with representational similarity analyses (RSA) of spatial patterns of brain activity has revealed reinstatement of recently-experienced events throughout a core memory retrieval network. In the present study, participants were scanned while they watched, immediately retrieved and then retrieved after a week, 24 short videos. Following the delayed retrieval, they freely recalled all videos outside of the scanner. We observed widespread within- and between-subject reinstatement effects within a posterior midline core memory retrieval network during all phases of the experiment. Within precuneus, bilateral middle temporal gyrus and the left hippocampus, reinstatement effects between the retrieval phases correlated with memory performance. These findings extend previous studies that have only employed short retention periods or highly rehearsed materials, demonstrating that memory representations for unique events are reliably reinstated over longer timeframes that are meaningful in the context of real-world episodic memory

Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep

Sleep is thought to play a complementary role in human memory processing: sleep loss impairs the formation of new memories during the following awake period and, conversely, normal sleep promotes the strengthening of the already encoded memories. However, whether sleep can strengthen deteriorated memories caused by insufficient sleep remains unknown. Here, we showed that sleep restriction in a group of participants caused a reduction in the stability of EEG activity patterns across multiple encoding of the same event during awake, compared with a group of participants that got a full night's sleep. The decrease of neural stability patterns in the sleep-restricted group was associated with higher slow oscillation-spindle coupling during a subsequent night of normal sleep duration, thereby suggesting the instantiation of restorative neural mechanisms adaptively supporting cognition and memory. Importantly, upon awaking, the two groups of participants showed equivalent retrieval accuracy supported by subtle differences in the reinstatement of encoding-related activity: it was longer lasting in sleep-restricted individuals than in controls. In addition, sustained reinstatement over time was associated with increased coupling between spindles and slow oscillations. Taken together, these results suggest that the strength of prior encoding might be an important moderator of memory consolidation during sleep. Supporting this view, spindles nesting in the slow oscillation increased the probability of correct recognition only for weakly encoded memories. Current results demonstrate the benefit that a full night's sleep can induce to impaired memory traces caused by an inadequate amount of sleep

Similarity Breeds Proximity: Pattern Similarity within and across Contexts Is Related to Later Mnemonic Judgments of Temporal Proximity

SummaryExperiences unfold over time, but little is known about the mechanisms that support the formation of coherent episodic memories for temporally extended events. Recent work in animals has provided evidence for signals in hippocampus that could link events across temporal gaps; however, it is unknown whether and how such signals might be related to later memory for temporal information in humans. We measured patterns of fMRI BOLD activity as people encoded items that were separated in time and manipulated the presence of shared or distinct context across items. We found that hippocampal pattern similarity in the BOLD response across trials predicted later temporal memory decisions when context changed. By contrast, pattern similarity in lateral occipital cortex was related to memory only when context remained stable. These data provide evidence in humans that representational stability in hippocampus across time may be a mechanism for temporal memory organization

Suppression weakens unwanted memories via a sustained reduction of neural reactivation

Aversive events sometimes turn into intrusive memories. However, prior evidence indicates that such memories can be controlled via a mechanism of retrieval suppression. Here, we test the hypothesis that suppression exerts a sustained influence on memories by deteriorating their neural representations. This deterioration, in turn, would hinder their subsequent reactivation and thus impoverish the vividness with which they can be recalled. In an fMRI study, participants repeatedly suppressed memories of aversive scenes. As predicted, this process rendered the memories less vivid. Using a pattern classifier, we observed that suppression diminished the neural reactivation of scene information both globally across the brain and locally in the parahippocampal cortices. Moreover, the decline in vividness was associated with reduced reinstatement of unique memory representations in right parahippocampal cortex. These results support the hypothesis that suppression weakens memories by causing a sustained reduction in the potential to reactivate their neural representations