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

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.

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Publication Details

Journal
PLoS Biology
Published
2025-11-25
DOI
https://doi.org/10.1371/journal.pbio.3003481
Primary Topic
Functional Brain Connectivity Studies
Type
article
Field-Weighted Citation Impact
0.00

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article

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

Eishi Asano, Peter Brunner, Stephan Schuele, Adam J. O. Dede et al.
PLoS Biology
Functional Brain Connectivity Studies
article

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

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

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.

PLoS BiologyVol. 23(11)
Northwestern University (US), Nationwide Children's Hospital (US), Mount Sinai Hospital (US), The University of Texas at Dallas (US), University of Calgary (CA), Wayne State University (US), Washington University in St. Louis (US), California Pacific Medical Center (US), Yale University (US), University of California San Diego (US), Rady Children's Hospital-San Diego (US), Michigan United (US), Lurie Children's Hospital (US), University of California, Davis (US), University of California, Berkeley (US), Stanford University (US)
Northwestern University, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Institute of Biomedical Imaging and Bioengineering, National Center for Advancing Translational Sciences
Openalex Percentile: Top 63%
Functional Brain Connectivity Studies
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