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

  1. Catherine M Sweeney-Reed  Is a corresponding author
  2. Tino Zaehle
  3. Jürgen Voges
  4. Friedhelm C Schmitt
  5. Lars Buentjen
  6. Klaus Kopitzki
  7. Hermann Hinrichs
  8. Hans-Jochen Heinze
  9. Michael D Rugg
  10. Robert T Knight
  11. Alan Richardson-Klavehn
  1. Otto von Guericke University, Germany
  2. University of Texas at Dallas, United States
  3. University of California, Berkeley, United States

Abstract

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.

Article and author information

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. Jürgen 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. Hermann Hinrichs

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

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

    Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas at Dallas, Dallas, United States
    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 (application number 0308), and all participants gave written informed consent in accordance with the Helsinki Declaration of 1975, as revised in 2000 and2008. Consent to participate in our study, as well as for publication of results in an anonymized format,was obtained by the neurosurgeon at the same time as consent was obtained for the surgicalprocedure.

Copyright

© 2015, 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.

Metrics

  • 1,596
    views
  • 379
    downloads
  • 34
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Catherine M Sweeney-Reed
  2. Tino Zaehle
  3. Jürgen Voges
  4. Friedhelm C Schmitt
  5. Lars Buentjen
  6. Klaus Kopitzki
  7. Hermann Hinrichs
  8. Hans-Jochen Heinze
  9. Michael D Rugg
  10. Robert T Knight
  11. Alan Richardson-Klavehn
(2015)
Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling
eLife 4:e07578.
https://doi.org/10.7554/eLife.07578

Share this article

https://doi.org/10.7554/eLife.07578

Further reading

    1. Neuroscience
    Maren Klingelhöfer-Jens, Katharina Hutterer ... Tina B Lonsdorf
    Research Article

    Childhood adversity is a strong predictor of developing psychopathological conditions. Multiple theories on the mechanisms underlying this association have been suggested which, however, differ in the operationalization of ‘exposure.’ Altered (threat) learning mechanisms represent central mechanisms by which environmental inputs shape emotional and cognitive processes and ultimately behavior. 1402 healthy participants underwent a fear conditioning paradigm (acquisition training, generalization), while acquiring skin conductance responses (SCRs) and ratings (arousal, valence, and contingency). Childhood adversity was operationalized as (1) dichotomization, and following (2) the specificity model, (3) the cumulative risk model, and (4) the dimensional model. Individuals exposed to childhood adversity showed blunted physiological reactivity in SCRs, but not ratings, and reduced CS+/CS- discrimination during both phases, mainly driven by attenuated CS+ responding. The latter was evident across different operationalizations of ‘exposure’ following the different theories. None of the theories tested showed clear explanatory superiority. Notably, a remarkably different pattern of increased responding to the CS- is reported in the literature for anxiety patients, suggesting that individuals exposed to childhood adversity may represent a specific sub-sample. We highlight that theories linking childhood adversity to (vulnerability to) psychopathology need refinement.

    1. Neuroscience
    William T Redman, Santiago Acosta-Mendoza ... Michael J Goard
    Research Article

    Although grid cells are one of the most well-studied functional classes of neurons in the mammalian brain, whether there is a single orientation and spacing value per grid module has not been carefully tested. We analyze a recent large-scale recording of medial entorhinal cortex to characterize the presence and degree of heterogeneity of grid properties within individual modules. We find evidence for small, but robust, variability and hypothesize that this property of the grid code could enhance the encoding of local spatial information. Performing analysis on synthetic populations of grid cells, where we have complete control over the amount heterogeneity in grid properties, we demonstrate that grid property variability of a similar magnitude to the analyzed data leads to significantly decreased decoding error. This holds even when restricted to activity from a single module. Our results highlight how the heterogeneity of the neural response properties may benefit coding and opens new directions for theoretical and experimental analysis of grid cells.