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.

Reviewing Editor

  1. Howard Eichenbaum, Boston University, United States

Publication history

  1. Received: March 19, 2015
  2. Accepted: May 19, 2015
  3. Accepted Manuscript published: May 20, 2015 (version 1)
  4. Version of Record published: June 8, 2015 (version 2)

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

  • 1,503
    Page views
  • 354
    Downloads
  • 24
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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
  1. Further reading

Further reading

    1. Neuroscience
    Frédéric Roux, George Parish ... Simon Hanslmayr
    Research Article

    Theta and gamma oscillations in the medial temporal lobe are suggested to play a critical role for human memory formation via establishing synchrony in neural assemblies. Arguably, such synchrony facilitates efficient information transfer between neurons and enhances synaptic plasticity, both of which benefit episodic memory formation. However, to date little evidence exists from humans that would provide direct evidence for such a specific role of theta and gamma oscillations for episodic memory formation. Here we investigate how oscillations shape the temporal structure of neural firing during memory formation in the medial temporal lobe. We measured neural firing and local field potentials in human epilepsy patients via micro-wire electrode recordings to analyze whether brain oscillations are related to co-incidences of firing between neurons during successful and unsuccessful encoding of episodic memories. The results show that phase-coupling of neurons to faster theta and gamma oscillations correlates with co-firing at short latencies (~20-30 ms) and occurs during successful memory formation. Phase-coupling at slower oscillations in these same frequency bands, in contrast, correlates with longer co-firing latencies and occurs during memory failure. Thus, our findings suggest that neural oscillations play a role for the synchronization of neural firing in the medial temporal lobe during the encoding of episodic memories.

    1. Developmental Biology
    2. Neuroscience
    Emily L Heckman, Chris Q Doe
    Research Advance

    The organization of neural circuits determines nervous system function. Variability can arise during neural circuit development (e.g. neurite morphology, axon/dendrite position). To ensure robust nervous system function, mechanisms must exist to accommodate variation in neurite positioning during circuit formation. Previously we developed a model system in the Drosophila ventral nerve cord to conditionally induce positional variability of a proprioceptive sensory axon terminal, and used this model to show that when we altered the presynaptic position of the sensory neuron, its major postsynaptic interneuron partner modified its dendritic arbor to match the presynaptic contact, resulting in functional synaptic input (Sales et al., 2019). Here we investigate the cellular mechanisms by which the interneuron dendrites detect and match variation in presynaptic partner location and input strength. We manipulate the presynaptic sensory neuron by (a) ablation; (b) silencing or activation; or (c) altering its location in the neuropil. From these experiments we conclude that there are two opposing mechanisms used to establish functional connectivity in the face of presynaptic variability: presynaptic contact stimulates dendrite outgrowth locally, whereas presynaptic activity inhibits postsynaptic dendrite outgrowth globally. These mechanisms are only active during an early larval critical period for structural plasticity. Collectively, our data provide new insights into dendrite development, identifying mechanisms that allow dendrites to flexibly respond to developmental variability in presynaptic location and input strength.