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Research Articles, Behavioral/Cognitive

Event Integration and Temporal Differentiation: How Hierarchical Knowledge Emerges in Hippocampal Subfields through Learning

Oded Bein and Lila Davachi
Journal of Neuroscience 6 March 2024, 44 (10) e0627232023; https://doi.org/10.1523/JNEUROSCI.0627-23.2023
Oded Bein
1Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08540
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Lila Davachi
2Department of Psychology, Columbia University, New York, New York 10027
3Center for Clinical Research, The Nathan S. Kline Institute for Psychiatric Research, Orangeburg, New York 10962
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Abstract

Everyday life is composed of events organized by changes in contexts, with each event containing an unfolding sequence of occurrences. A major challenge facing our memory systems is how to integrate sequential occurrences within events while also maintaining their details and avoiding over-integration across different contexts. We asked if and how distinct hippocampal subfields come to hierarchically and, in parallel, represent both event context and subevent occurrences with learning. Female and male human participants viewed sequential events defined as sequences of objects superimposed on shared color frames while undergoing high-resolution fMRI. Importantly, these events were repeated to induce learning. Event segmentation, as indexed by increased reaction times at event boundaries, was observed in all repetitions. Temporal memory decisions were quicker for items from the same event compared to across different events, indicating that events shaped memory. With learning, hippocampal CA3 multivoxel activation patterns clustered to reflect the event context, with more clustering correlated with behavioral facilitation during event transitions. In contrast, in the dentate gyrus (DG), temporally proximal items that belonged to the same event became associated with more differentiated neural patterns. A computational model explained these results by dynamic inhibition in the DG. Additional similarity measures support the notion that CA3 clustered representations reflect shared voxel populations, while DG’s distinct item representations reflect different voxel populations. These findings suggest an interplay between temporal differentiation in the DG and attractor dynamics in CA3. They advance our understanding of how knowledge is structured through integration and separation across time and context.

  • attractor dynamics
  • CA3
  • dentate gyrus
  • encoding
  • event segmentation
  • high-resolution fMRI
  • hippocampus
  • learning
  • pattern completion
  • pattern separation

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The Journal of Neuroscience: 44 (10)
Journal of Neuroscience
Vol. 44, Issue 10
6 Mar 2024
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Event Integration and Temporal Differentiation: How Hierarchical Knowledge Emerges in Hippocampal Subfields through Learning
Oded Bein, Lila Davachi
Journal of Neuroscience 6 March 2024, 44 (10) e0627232023; DOI: 10.1523/JNEUROSCI.0627-23.2023

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Event Integration and Temporal Differentiation: How Hierarchical Knowledge Emerges in Hippocampal Subfields through Learning
Oded Bein, Lila Davachi
Journal of Neuroscience 6 March 2024, 44 (10) e0627232023; DOI: 10.1523/JNEUROSCI.0627-23.2023
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Keywords

  • attractor dynamics
  • CA3
  • dentate gyrus
  • encoding
  • event segmentation
  • high-resolution fMRI
  • hippocampus
  • learning
  • pattern completion
  • pattern separation

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