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

  1. Catherine M Sweeney-Reed  Is a corresponding author
  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
  1. Otto von Guericke University, Germany
  2. University of California, Berkeley, United States
Research Article
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Cite this article as: eLife 2014;3:e05352 doi: 10.7554/eLife.05352

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.

Reviewing Editor

  1. Howard Eichenbaum, Boston University, United States

Publication history

  1. Received: October 27, 2014
  2. Accepted: December 22, 2014
  3. Accepted Manuscript published: December 23, 2014 (version 1)
  4. Version of Record published: January 22, 2015 (version 2)

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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Further reading

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    Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling

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    Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (Sweeney-Reed et al., 2014). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

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