An Enduring Role for Hippocampal Pattern Completion in Addition to an Emergent Nonhippocampal Contribution to Holistic Episodic Retrieval after a 24†h Delay.

Episodic memory retrieval is associated with the holistic neocortical reinstatement of all event information, an effect driven by hippocampal pattern completion. However, whether holistic reinstatement occurs, and whether hippocampal pattern completion continues to drive reinstatement, after a period of consolidation is unclear. Theories of systems consolidation predict either a time-variant or time-invariant role of the hippocampus in the holistic retrieval of episodic events. Here, we assessed whether episodic events continue to be reinstated holistically and whether hippocampal pattern completion continues to facilitate holistic reinstatement following a period of consolidation. Female and male human participants learned "events" that comprised multiple overlapping pairs of event elements (e.g., person-location, object-location, location-person). Importantly, encoding occurred either immediately before or 24 h before retrieval. Using fMRI during the retrieval of events, we show evidence for holistic reinstatement, as well as a correlation between reinstatement and hippocampal pattern completion, regardless of whether retrieval occurred immediately or 24 h after encoding. Thus, hippocampal pattern completion continues to contribute to holistic reinstatement after a delay. However, our results also revealed that some holistic reinstatement can occur without evidence for a corresponding signature of hippocampal pattern completion after a delay (but not immediately after encoding). We therefore show that hippocampal pattern completion, in addition to a nonhippocampal process, has a role in holistic reinstatement following a period of consolidation. Our results point to a consolidation process where the hippocampus and neocortex may work in an additive, rather than compensatory, manner to support episodic memory retrieval.

Hippocampal theta activity during encoding promotes subsequent associative memory in humans.

Hippocampal theta oscillations have been implicated in associative memory in humans. However, findings from electrophysiological studies using scalp electroencephalography or magnetoencephalography, and those using intracranial electroencephalography are mixed. Here we asked 10 pre-surgical epilepsy patients undergoing intracranial electroencephalography recording, along with 21 participants undergoing magnetoencephalography recordings, to perform an associative memory task, and examined whether hippocampal theta activity during encoding was predictive of subsequent associative memory performance. Across the intracranial electroencephalography and magnetoencephalography studies, we observed that theta power in the hippocampus increased during encoding, and that this increase differed as a function of subsequent memory, with greater theta activity for pairs that were successfully retrieved in their entirety compared with those that were not remembered. This helps to clarify the role of theta oscillations in associative memory formation in humans, and further, demonstrates that findings in epilepsy patients undergoing intracranial electroencephalography recordings can be extended to healthy participants undergoing magnetoencephalography recordings.

Targeted memory reactivation during sleep can induce forgetting of overlapping memories.

Memory reactivation during sleep can shape new memories into a long-term form. Reactivation of memories can be induced via the delivery of auditory cues during sleep. Although this targeted memory reactivation (TMR) approach can strengthen newly acquired memories, research has tended to focus on single associative memories. It is less clear how TMR affects retention for overlapping associative memories. This is critical, given that repeated retrieval of overlapping associations during wake can lead to forgetting, a phenomenon known as retrieval-induced forgetting (RIF). We asked whether a similar pattern of forgetting occurs when TMR is used to cue reactivation of overlapping pairwise associations during sleep. Participants learned overlapping pairs-learned separately, interleaved with other unrelated pairs. During sleep, we cued a subset of overlapping pairs using TMR. While TMR increased retention for the first encoded pairs, memory decreased for the second encoded pairs. This pattern of retention was only present for pairs not tested prior to sleep. The results suggest that TMR can lead to forgetting, an effect similar to RIF during wake. However, this effect did not extend to memories that had been strengthened via retrieval prior to sleep. We therefore provide evidence for a reactivation-induced forgetting effect during sleep.

Forgetting across a hierarchy of episodic representations.

Rich episodic experiences are represented in a hierarchical manner across a diverse network of brain regions, and as such, the way in which episodes are forgotten is likely to be similarly diverse. Using novel experimental approaches and statistical modelling, recent research has suggested that item-based representations, such as ones related to the colour and shape of an object, fragment over time, whereas higher-order event-based representations may be forgotten in a more 'holistic' uniform manner. We propose a framework that reconciles these findings, where complex episodes are represented in a hierarchical manner, from individual items, to small-scale events, to large-scale episodic narratives. Each level in the hierarchy is represented in distinct brain regions, from the perirhinal cortex, to posterior hippocampus, to anterior hippocampus and ventromedial prefrontal cortex. Critically, forgetting may be underpinned by different mechanisms at each level in the hierarchy, leading to different patterns of behaviour.

Tracking the Emergence of Location-based Spatial Representations in Human Scene-Selective Cortex.

Scene-selective regions of the human brain form allocentric representations of locations in our environment. These representations are independent of heading direction and allow us to know where we are regardless of our direction of travel. However, we know little about how these location-based representations are formed. Using fMRI representational similarity analysis and linear mixed models, we tracked the emergence of location-based representations in scene-selective brain regions. We estimated patterns of activity for two distinct scenes, taken before and after participants learnt they were from the same location. During a learning phase, we presented participants with two types of panoramic videos: (1) an overlap video condition displaying two distinct scenes (0° and 180°) from the same location and (2) a no-overlap video displaying two distinct scenes from different locations (which served as a control condition). In the parahippocampal cortex (PHC) and retrosplenial cortex (RSC), representations of scenes from the same location became more similar to each other only after they had been shown in the overlap condition, suggesting the emergence of viewpoint-independent location-based representations. Whereas these representations emerged in the PHC regardless of task performance, RSC representations only emerged for locations where participants could behaviorally identify the two scenes as belonging to the same location. The results suggest that we can track the emergence of location-based representations in the PHC and RSC in a single fMRI experiment. Further, they support computational models that propose the RSC plays a key role in transforming viewpoint-independent representations into behaviorally relevant representations of specific viewpoints.

United we fall: All-or-none forgetting of complex episodic events.

Do complex event representations fragment over time, or are they instead forgotten in an all-or-none manner? For example, if we met a friend in a café and they gave us a present, do we forget the constituent elements of this event (location, person, and object) independently, or would the whole event be forgotten? Research suggests that item-based memories are forgotten in a fragmented manner. However, we do not know how more complex episodic, event-based memories are forgotten. We assessed both retrieval accuracy and dependency-the statistical association between the retrieval successes of different elements from the same event-for complex events. Across 4 experiments, we show that retrieval dependency is found both immediately after learning and following a 12-hr and 1-week delay. Further, the amount of retrieval dependency after a delay is greater than that predicted by a model of independent forgetting. This dependency was only seen for coherent "closed-loops," where all pairwise associations between locations, people, and objects were encoded. When "open-loops" were learned, where only 2 out of the 3 possible associations were encoded, no dependency was seen immediately after learning or after a delay. Finally, we also provide evidence for higher retention rates for closed-loops than for open-loops. Therefore, closed-loops do not fragment as a function of forgetting and are retained for longer than are open-loops. Our findings suggest that coherent episodic events are not only retrieved, but also forgotten, in an all-or-none manner. (PsycINFO Database Record (c) 2020 APA, all rights reserved).