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Review
. 2019 Mar;29(3):162-183.
doi: 10.1002/hipo.23074. Epub 2019 Feb 7.

Transcending time in the brain: How event memories are constructed from experience

David Clewett  1 , Sarah DuBrow  2 , Lila Davachi  3   4
Affiliations
Review

Transcending time in the brain: How event memories are constructed from experience

David Clewett et al. Hippocampus. 2019 Mar.

Abstract

Our daily lives unfold continuously, yet when we reflect on the past, we remember those experiences as distinct and cohesive events. To understand this phenomenon, early investigations focused on how and when individuals perceive natural breakpoints, or boundaries, in ongoing experience. More recent research has examined how these boundaries modulate brain mechanisms that support long-term episodic memory. This work has revealed that a complex interplay between hippocampus and prefrontal cortex promotes the integration and separation of sequential information to help organize our experiences into mnemonic events. Here, we discuss how both temporal stability and change in one's thoughts, goals, and surroundings may provide scaffolding for these neural processes to link and separate memories across time. When learning novel or familiar sequences of information, dynamic hippocampal processes may work both independently from and in concert with other brain regions to bind sequential representations together in memory. The formation and storage of discrete episodic memories may occur both proactively as an experience unfolds. They may also occur retroactively, either during a context shift or when reactivation mechanisms bring the past into the present to allow integration. We also describe conditions and factors that shape the construction and integration of event memories across different timescales. Together these findings shed new light on how the brain transcends time to transform everyday experiences into meaningful memory representations.

Keywords: context; episodic memory; event segmentation; events; hippocampus; integration; prefrontal cortex; temporal context; time.

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Figures

Figure 1
Figure 1
The diverse effects of various context shifts, or event boundaries, on different episodic memory outcomes. Experiencing a shift in the current context, such as moving from a park to a city street, can cause individuals to perceive a boundary between one episode and the next. In the long-term, this boundary influences how those prior episodes become represented and organized in memory, with different influences on both the temporal and non-temporal aspects of episodic memory.
Figure 2
Figure 2
Remembering items as appearing closer together relates to more stable encoding patterns of hippocampal activity across time. (A) In this fMRI study, participants view a series of images that were organized as “quartets.” A face or object was paired with a scene that either remained the same for four trials (same context condition) or switched after two trials (boundary context condition), creating a stable or less stable context, respectively. Memory was then tested for the temporal distance between items as well as source memory for an item and its paired scene. (B) Results showed that participants were more likely to remember items from the same context as appearing closer together in the sequence; by contrast, participants were more likely to remember items that had spanned a context shift as having appeared farther apart in the sequence. (C) Ratings of closer temporal proximity were associated with greater hippocampal pattern similarity across event boundaries (adapted from Ezzyat & Davachi, 2014).
Figure 3
Figure 3
Local and global patterns of hippocampal and prefrontal cortex (PFC) activity/connectivity differentially relate to serial recall of items encountered within versus across events. (A/B) Following a sequence-learning paradigm, participants were more likely to accurately report an item and then its successor if those items had appeared within the same context (i.e., were both faces) compared to if those items that had spanned an event boundary. (B) Participants were also more likely to ‘jump’ to an event boundary during free recall, suggesting that context shifts enhance the memory strength of items constituting a boundary. (C) FMRI analyses revealed that the successful serial recall of items that spanned a context shift were associated with increased univariate BOLD signal in the lateral PFC. (D) Successful serial recall of items encoded within the same context was instead associated with increased functional connectivity between the hippocampus and medial PFC (adapted from DuBrow & Davachi, 2016).
Figure 4
Figure 4
Post-event hippocampal and striatal activity relate to successful memory of just-experienced events. (A) At the offset of a naturalistic video clip, there is an increase in hippocampal and striatal activity that relates to better associative memory for details of that prior event (right panel). These post-event neural signals were not observed for recent scrambled videos and less so for forgotten information, suggesting that these mnemonic processes relate to the integration of meaningful episodic memory representations (adapted from Ben-Yakov and Dudai, 2011).
Figure 5
Figure 5
Summary of neural processes that support proactive and retroactive memory integration at shorter timescales. Different cognitive and neural processes are engaged either proactively as time unfolds (1 and 2) or retroactively when a context shift occurs (3 and 4; top panel). (1 and 2) First, memory integration can be facilitated by contextual overlap, either through (1) the extraction of statistical regularities as experiences unfold (e.g., contiguities in space, item color etc.) or (2) familiarity with a given sequence. In the latter, hippocampal forward prediction signals and its functional connectivity with mPFC may prime representations of learned sequences, providing the contextual and representational overlap that facilitates integration. Together, these neural processes may allocate context-appropriate information to a meaningful memory representation. (3) Although event boundaries typically impair temporal order memory, the immediate retrieval of pre-boundary information via PFC and hippocampal activity may counter these effects. This process may help to maintain a sense of continuity despite context changes (greenish hue persists into what would otherwise be represented as Episode 2). Goal-directed attention and associative learning strategies may trigger these processes that preserve memory integration across time. (4) Neural reactivation or replay processes in hippocampus, frontoparietal networks, and basal ganglia at a context shift might also retroactively integrate recent information into a coherent memory representation.
Figure 6
Figure 6
Context shifts, such as a scene image inserted between two faces, may accelerate the drift of a slowly evolving temporal context signal (red rectangle) that may reside in MTL structures and the PFC. In turn, sequential stimuli (faces) separated by a short lag become embedded in more distinct temporal contexts. This lack of contextual overlap relates to order memory impairments between two items (faces) that spanned a context shift (scene).
Figure 7
Figure 7
Effects of temporal context and proximity on hippocampal pattern integration versus separation. Separate learning events that occur within a specific time window (e.g., minutes-to-hours) may become integrated in memory. During learning, a distinct subset of neurons represents a specific context/memory (left panel; yellow dots). Up to 5 hours later, those neurons remain residually active (dim yellow dots) and may overlap with a subsequent event active. This similar but new learning episode (middle panel; purple dots) may lead to the recruitment of these overlapping hippocampal neuronal ensembles, so that these two events become linked in behavior (middle panel; yellow/purple combination dots). Across very long delays (days), hippocampal ensembles may become more differentiated despite representing similar spatial or perceptual contexts, including revisiting the same space (right panel; blue dots).
Figure 8
Figure 8
Memory tradeoffs between source memory-binding and temporal order memory elicited by event boundaries. (A) In this behavioral study, participants studied sequences with items displayed on a background colors. ‘Events’ were defined as 6 successive items with the same colored background, with each event being followed by a color switch, or event boundary. Participants were instructed to rate the pleasantness of each item-color pairing when each appeared. Following a list of 36 items, memory was tested for the background color of each object as well as the order between two items that were always the same temporal distance apart. (B) Results revealed that context shifts had different effects on source memory and temporal order memory, with shifts enhancing source memory for boundary items but impairing temporal memory for item pairs that had an intervening color switch. C) A tertiary split was performed on reaction times for the color pleasantness ratings during encoding and then further broken down by source memory accuracy for those items. Faster reaction times to event boundary items were associated with better source memory for the background colors. This finding suggests that greater attention to boundary representations was related to strong source memory binding for those items (adapted from Heusser et al., 2018).
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