Corticothalamic phase synchrony and cross-frequency coupling predict human memory formation

Abstract

The anterior thalamic nucleus (ATN) is thought to play an important role in a brain network involving the hippocampus and neocortex, which enables human memories to be formed. However, its small size and location deep within the brain have impeded direct investigation in humans with non-invasive techniques. Here we provide direct evidence for a functional role for the ATN in memory formation from rare simultaneous human intrathalamic and scalp electroencephalogram (EEG) recordings from 8 volunteering patients receiving intrathalamic electrodes implanted for the treatment of epilepsy, demonstrating real-time communication between neocortex and ATN during successful memory encoding. Neocortical-ATN theta oscillatory phase synchrony of local field potentials and neocortical-theta-to-ATN-gamma cross-frequency coupling during presentation of complex photographic scenes predicted later memory for the pictures, demonstrating a key role for the ATN in human memory encoding.

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Author details

  1. Catherine M Sweeney-Reed

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    For correspondence
    catherine.sweeney-reed@med.ovgu.de
    Competing interests
    The authors declare that no competing interests exist.
  2. Tino Zaehle

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Juergen Voges

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Friedhelm C Schmitt

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Lars Buentjen

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Klaus Kopitzki

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Christine Esslinger

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Hermann Hinrichs

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Hans-Jochen Heinze

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Robert T Knight

    Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Alan Richardson-Klavehn

    Department of Neurology, Otto von Guericke University, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Human subjects: The measurements were approved by the Ethics Commission of the Medical Faculty of the Otto-von-Guericke University, Magdeburg, and all participants gave written informed consent.

Copyright

© 2014, Sweeney-Reed et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Catherine M Sweeney-Reed
  2. Tino Zaehle
  3. Juergen Voges
  4. Friedhelm C Schmitt
  5. Lars Buentjen
  6. Klaus Kopitzki
  7. Christine Esslinger
  8. Hermann Hinrichs
  9. Hans-Jochen Heinze
  10. Robert T Knight
  11. Alan Richardson-Klavehn
(2014)
Corticothalamic phase synchrony and cross-frequency coupling predict human memory formation
eLife 3:e05352.
https://doi.org/10.7554/eLife.05352

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https://doi.org/10.7554/eLife.05352