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Cognitive boundary signals in the human medial temporal lobe shape episodic memory representation

Zheng, Jie and Schjetnan, Andrea Gómez Palacio and Yebra, Mar and Mosher, Clayton and Kalia, Suneil and Valiante, Taufik A. and Mamelak, Adam N. and Kreiman, Gabriel and Rutishauser, Ueli (2021) Cognitive boundary signals in the human medial temporal lobe shape episodic memory representation. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20210119-132232653

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Abstract

While experience unfolds continuously, memories are organized as a set of discrete events that bind together the “where”, “when”, and “what” of episodic memory. This segmentation of continuous experience is thought to be facilitated by the detection of salient environmental or cognitive events. However, the underlying neural mechanisms and how such segmentation shapes episodic memory representations remain unclear. We recorded from single neurons in the human medial temporal lobe while subjects watched videos with different types of embedded boundaries and were subsequently evaluated for memories of the video contents. Here we show neurons that signal the presence of cognitive boundaries between subevents from the same episode and neurons that detect the abstract separation between different episodes. The firing rate and spike timing of these boundary-responsive neurons were predictive of later memory retrieval accuracy. At the population level, abrupt neural state changes following boundaries predicted enhanced memory strength but impaired order memory, capturing the behavioral tradeoff subjects exhibited when recalling episodic content versus temporal order. Successful retrieval was associated with reinstatement of the neural state present following boundaries, indicating that boundaries structure memory search. These findings reveal a neuronal substrate for detecting cognitive boundaries and show that cognitive boundary signals facilitate the mnemonic organization of continuous experience as a set of discrete episodic events.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.01.16.426538DOIDiscussion Paper
ORCID:
AuthorORCID
Kalia, Suneil0000-0003-2054-1915
Valiante, Taufik A.0000-0002-3443-3790
Mamelak, Adam N.0000-0002-4245-6431
Rutishauser, Ueli0000-0002-9207-7069
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This version posted January 16, 2021. We thank Mengmi Zhang, Jan Kaminski and other members from Rutishauser and Kreiman lab for discussion; Nand Chandravadia and Victoria Barkely for data transferring and organization; Chrystal Reed, Jeffrey Chung, and the clinical teams at both Cedars-Sinai Medical Center and Toronto Western Hospital. We especially indebted to the patient volunteers who participated in this study. This work was supported by the Brain Canada program (to A.GPS.) and NIH U01NS103792 (to U.R.). Data and Code availability: Data and analytic code that support the findings of this study will be deposited at Open Science Framework upon acceptance. Author contributions: J.Z. conceived the project. J.Z., G.K. and U.R. contributed ideas for experiments and analysis. V.T. and A.M. managed patients and surgeries; J.Z., A.GPS., M. Y. and C. M. collected data; J.Z. performed the analyses; J.Z., G.K. and U.R. wrote the manuscript with input from all authors. Authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Brain Canada ProgramUNSPECIFIED
NIHU01NS103792
Record Number:CaltechAUTHORS:20210119-132232653
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210119-132232653
Official Citation:Cognitive boundary signals in the human medial temporal lobe shape episodic memory representation. Jie Zheng, Andrea Gómez Palacio Schjetnan, Mar Yebra, Clayton Mosher, Suneil Kalia, Taufik A. Valiante, Adam N. Mamelak, Gabriel Kreiman, Ueli Rutishauser. bioRxiv 2021.01.16.426538; doi: https://doi.org/10.1101/2021.01.16.426538
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:107546
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:19 Jan 2021 21:37
Last Modified:19 Jan 2021 21:37

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