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Theta mediated dynamics of human hippocampal-neocortical learning systems in memory formation and retrieval

Sandra Gattas, Myra Sarai Larson, Lilit Mnatsakanyan, Indranil Sen-Gupta, Sumeet Vadera, Lee Swindlehurst, Paul E. Rapp, Jack J. Lin, View ORCID ProfileMichael A. Yassa
doi: https://doi.org/10.1101/2023.09.20.558688
Sandra Gattas
1Department of Electrical Engineering and Computer Science, School of Engineering, University of California, Irvine, Irvine, CA, 92617, USA
2Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California, 92697, USA
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Myra Sarai Larson
2Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California, 92697, USA
3Department of Neurobiology and Behavior, School of Biological Sciences, University of California, Irvine, Irvine, CA, 92697, USA
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Lilit Mnatsakanyan
4Department of Neurology, School of Medicine, University of California, Irvine, CA, 92697, USA
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Indranil Sen-Gupta
4Department of Neurology, School of Medicine, University of California, Irvine, CA, 92697, USA
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Sumeet Vadera
5Department of Neurological Surgery, School of Medicine, University of California, Irvine, Irvine, CA, 92697, USA
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Lee Swindlehurst
1Department of Electrical Engineering and Computer Science, School of Engineering, University of California, Irvine, Irvine, CA, 92617, USA
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Paul E. Rapp
6Department of Military & Emergency Medicine, Uniformed Services University, Bethesda, MD, 20814, USA
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Jack J. Lin
2Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California, 92697, USA
4Department of Neurology, School of Medicine, University of California, Irvine, CA, 92697, USA
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Michael A. Yassa
2Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California, 92697, USA
3Department of Neurobiology and Behavior, School of Biological Sciences, University of California, Irvine, Irvine, CA, 92697, USA
4Department of Neurology, School of Medicine, University of California, Irvine, CA, 92697, USA
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  • ORCID record for Michael A. Yassa
  • For correspondence: michael.yassa@uci.edu
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Abstract

Episodic memory arises as a function of dynamic interactions between the hippocampus and the neocortex, yet the mechanisms have remained elusive. Here, using human intracranial recordings during a mnemonic discrimination task, we report that 4-5 Hz (theta) power is differentially recruited during discrimination vs. overgeneralization, and its phase supports hippocampal-neocortical when memories are being formed and correctly retrieved. Interactions were largely bidirectional, with small but significant net directional biases; a hippocampus-to-neocortex bias during acquisition of new information that was subsequently correctly discriminated, and a neocortex-to-hippocampus bias during accurate discrimination of new stimuli from similar previously learned stimuli. The 4-5 Hz rhythm may facilitate the initial stages of information acquisition by neocortex during learning and the recall of stored information from cortex during retrieval. Future work should further probe these dynamics across different types of tasks and stimuli and computational models may need to be expanded accordingly to accommodate these findings.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://osf.io/dn9as/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 22, 2023.
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Theta mediated dynamics of human hippocampal-neocortical learning systems in memory formation and retrieval
Sandra Gattas, Myra Sarai Larson, Lilit Mnatsakanyan, Indranil Sen-Gupta, Sumeet Vadera, Lee Swindlehurst, Paul E. Rapp, Jack J. Lin, Michael A. Yassa
bioRxiv 2023.09.20.558688; doi: https://doi.org/10.1101/2023.09.20.558688
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Theta mediated dynamics of human hippocampal-neocortical learning systems in memory formation and retrieval
Sandra Gattas, Myra Sarai Larson, Lilit Mnatsakanyan, Indranil Sen-Gupta, Sumeet Vadera, Lee Swindlehurst, Paul E. Rapp, Jack J. Lin, Michael A. Yassa
bioRxiv 2023.09.20.558688; doi: https://doi.org/10.1101/2023.09.20.558688

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