# Episodic memory involves transient and sparse connectivity aligned to both internal and external events

**Authors:** Adam J. O. Dede, Zachariah R. Cross, Samantha M. Gray, Joseph P. Kelly, Qin Yin, Parisa Vahidi, Eishi Asano, Stephan U. Schuele, Joshua M. Rosenow, Joyce Y. Wu, Sandi K. Lam, Jeffrey S. Raskin, Jack J. Lin, Olivia Kim McManus, Shifteh Sattar, Ammar Shaikhouni, David King-Stephens, Peter B. Weber, Kenneth D. Laxer, Peter Brunner, Jarod L. Roland, Ignacio Saez, Fady Girgis, Robert T. Knight, Noa Ofen, Elizabeth L. Johnson

PMC · DOI: 10.1371/journal.pbio.3003481 · 2025-11-25

## TL;DR

This study shows that episodic memory relies on short-lived, sparsely connected brain states that change between encoding and retrieval.

## Contribution

The study reveals dynamic shifts in brain connectivity and timing between encoding and retrieval of episodic memories.

## Key findings

- PFC-MTL theta connectivity is aligned with internal PFC peaks during encoding and external stimuli during retrieval.
- Anterior cingulate cortex connectivity is aligned only with internal HFB peaks, indicating an evaluative role.
- Successful memory performance is linked to transient, sparse whole-brain network states.

## Abstract

Episodic memory depends on the coordination of local processing, indexed by high-frequency broadband (HFB) activity, with global organization, indexed by theta oscillations. However, theta and HFB exhibit asynchronous timing, raising the question of how results of local processing are communicated. Using intracranial EEG in patients performing a recognition memory task, we examined this coordination across medial temporal (MTL) and prefrontal (PFC) regions. HFB peaks occurred earlier in the MTL than in the PFC. Contrasting analyses were anchored either to these internally driven HFB peaks or to the external event of stimulus presentation. We discovered three key results. First, the role of the PFC changed from encoding to retrieval. Specifically, PFC-MTL theta connectivity was aligned with internal PFC peaks during encoding, suggesting top-down initiation. By contrast, this connection was aligned with external stimulus presentation during retrieval, suggesting bottom-up initiation. Second, the anterior cingulate cortex exhibited connectivity that was aligned to internal HFB peaks only, suggesting that its role is evaluative, devoid of direct stimulus processing. Third, graph theoretic analysis of whole-brain connectivity patterns revealed that the connections predicting successful memory performance were embedded in transient, sparse network states. These results reveal that analyses triggered from internally-generated events yield different results when compared to classic analyses triggered using external events. The picture that emerges is a sequence of specific, short-lived, internally-generated states that drive episodic memory success.

Episodic memory depends on the coordination of local processing with global organization. This study reveals that episodic memory relies on brief, sparsely connected brain states coordinated across medial temporal and prefrontal regions, uncovering dynamic shifts in network directionality and timing between encoding and retrieval.

## Full-text entities

- **Species:** Homo sapiens (human, species) [taxon 9606]

## Figures

27 figures with captions in the complete paper: https://tomesphere.com/paper/PMC12646405/full.md

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Source: https://tomesphere.com/paper/PMC12646405