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Neurons detect cognitive boundaries to structure episodic memories in humans

Zheng, Jie and Schjetnan, Andrea G. P. and Yebra, Mar and Gomes, Bernard A. and Mosher, Clayton P. and Kalia, Suneil K. and Valiante, Taufik A. and Mamelak, Adam N. and Kreiman, Gabriel and Rutishauser, Ueli (2022) Neurons detect cognitive boundaries to structure episodic memories in humans. Nature Neuroscience, 25 (3). pp. 358-368. ISSN 1097-6256. doi:10.1038/s41593-022-01020-w. https://resolver.caltech.edu/CaltechAUTHORS:20210119-132232653

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Abstract

While experience is continuous, memories are organized as discrete events. Cognitive boundaries are thought to segment experience and structure memory, but how this process is implemented remains unclear. We recorded the activity of single neurons in the human medial temporal lobe (MTL) during the formation and retrieval of memories with complex narratives. Here, we show that neurons responded to abstract cognitive boundaries between different episodes. Boundary-induced neural state changes during encoding predicted subsequent recognition accuracy but impaired event order memory, mirroring a fundamental behavioral tradeoff between content and time memory. Furthermore, the neural state following boundaries was reinstated during both successful retrieval and false memories. These findings reveal a neuronal substrate for detecting cognitive boundaries that transform experience into mnemonic episodes and structure mental time travel during retrieval.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41593-022-01020-wDOIArticle
https://rdcu.be/cIWnUPublisherFree ReadCube access
https://doi.org/10.1101/2021.01.16.426538DOIDiscussion Paper
https://doi.org/10.48324/dandi.000207/0.220216.0323DOIData
https://github.com/rutishauserlab/cogboundary-zhengRelated ItemCode
ORCID:
AuthorORCID
Zheng, Jie0000-0002-9086-3760
Schjetnan, Andrea G. P.0000-0002-4319-7689
Yebra, Mar0000-0001-8445-1893
Gomes, Bernard A.0000-0002-2803-964X
Mosher, Clayton P.0000-0002-9213-3059
Kalia, Suneil K.0000-0003-2054-1915
Valiante, Taufik A.0000-0002-3443-3790
Mamelak, Adam N.0000-0002-4245-6431
Kreiman, Gabriel0000-0003-3505-8475
Rutishauser, Ueli0000-0002-9207-7069
Alternate Title:Cognitive boundary signals in the human medial temporal lobe shape episodic memory representation
Additional Information:© 2022 Nature Publishing Group. Received 01 March 2021; Accepted 19 January 2022; Published 07 March 2022. We thank C. Katz and K. Patel for helping set up the recording system for single-unit recordings at Toronto Western Hospital, N. Chandravadia and V. Barkely for data transferring and organization, C. Reed, J. Chung and the clinical teams at both Cedars-Sinai Medical Center and Toronto Western Hospital and M. Zhang, J. Kaminski and other members of the Rutishauser and Kreiman labs for discussion. We are especially indebted to the volunteers who participated in this study. This work was supported by NIH U01NS103792 and U01NS117839 (to U.R.), NSF 1231216 (G.K.) and Brain Canada (to T.A.V.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Data availability: The data (in NWB format) that supports the key findings of this study are publicly available on the DANDI archive (https://doi.org/10.48324/dandi.000207/0.220216.0323). Code availability: Codes that support the key findings of this study are publicly available on GitHub (https://github.com/rutishauserlab/cogboundary-zheng). Contributions: J.Z. conceived the project. J.Z., G.K. and U.R. contributed ideas for experiments and analysis. S.K.K., T.A.V. and A.N.M. managed participants and surgeries. J.Z., A.G.P.S., M. Y. and C.P.M. collected data. J.Z. performed the analyses. B.A.G. performed electrode localization. B.A.G., J.Z. and U.R. and produced the Neurodata Without Borders (NWB) formatted dataset for public release. J.Z., G.K. and U.R. wrote the manuscript with input from all authors. The authors declare no competing interests. Peer review information: Nature Neuroscience thanks Christopher Baldassano and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Funders:
Funding AgencyGrant Number
NIHU01NS103792
NIHU01NS117839
NSFDBI-1231216
Brain CanadaUNSPECIFIED
Subject Keywords:Cognitive neuroscience; Long-term memory; Neurophysiology
Issue or Number:3
DOI:10.1038/s41593-022-01020-w
Record Number:CaltechAUTHORS:20210119-132232653
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210119-132232653
Official Citation:Zheng, J., Schjetnan, A.G.P., Yebra, M. et al. Neurons detect cognitive boundaries to structure episodic memories in humans. Nat Neurosci 25, 358–368 (2022). https://doi.org/10.1038/s41593-022-01020-w
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:14 Mar 2022 22:15

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