Oscillations support short latency co-firing of neurons during human episodic memory formation

  1. Frédéric Roux
  2. George Parish
  3. Ramesh Chelvarajah
  4. David T Rollings
  5. Vijay Sawlani
  6. Hajo Hamer
  7. Stephanie Gollwitzer
  8. Gernot Kreiselmeyer
  9. Marije J ter Wal
  10. Luca Kolibius
  11. Bernhard P Staresina
  12. Maria Wimber
  13. Matthew W Self
  14. Simon Hanslmayr  Is a corresponding author
  1. University of Birmingham, United Kingdom
  2. Queen Elizabeth Hospital Birmingham, United Kingdom
  3. University Hospital Erlangen, Germany
  4. University of Glasgow, United Kingdom
  5. Netherlands Institute for Neuroscience, Netherlands

Abstract

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.

Data availability

All code used for data analysis and visualization of results is deposited here: https://osf.io/fngz8/

The following data sets were generated

Article and author information

Author details

  1. Frédéric Roux

    School of Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. George Parish

    Department of Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7533-8298
  3. Ramesh Chelvarajah

    Neuroscience Department, Queen Elizabeth Hospital Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. David T Rollings

    Neuroscience Department, Queen Elizabeth Hospital Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Vijay Sawlani

    Neuroscience Department, Queen Elizabeth Hospital Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Hajo Hamer

    Department of Neurology, University Hospital Erlangen, Erlangen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Stephanie Gollwitzer

    Department of Neurology, University Hospital Erlangen, Erlangen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Gernot Kreiselmeyer

    Department of Neurology, University Hospital Erlangen, Erlangen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Marije J ter Wal

    School of Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4922-3435
  10. Luca Kolibius

    Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Bernhard P Staresina

    Department of Experimental Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0558-9745
  12. Maria Wimber

    Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1917-353X
  13. Matthew W Self

    Department of Vision and Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5731-579X
  14. Simon Hanslmayr

    Institute for Neuroscience and Psychology, University of Glasgow, Glasgow, United Kingdom
    For correspondence
    simon.hanslmayr@glasgow.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4448-2147

Funding

European Research Council (647954)

  • Simon Hanslmayr

Economic and Social Research Council (ES/R010072/1)

  • Simon Hanslmayr

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Informed consent to participate in the experiments and consent to publish the results was obtained from the patients prior to data collection. Ethical approvals were given by National Research Ethics Service (NRES), Research Ethics Committee (Nr. 15/WM/0219), the ethical review board of the Friedrich-Alexander Universität Erlangen-Nürnberg (Nr. 124_12 B), and the Medical Ethical Review board of the Vrije Universiteit Medisch Centrum (Nr. NL55554.029.15), for Birmingham, Erlangen and Amsterdam respectively.

Copyright

© 2022, Roux 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. Frédéric Roux
  2. George Parish
  3. Ramesh Chelvarajah
  4. David T Rollings
  5. Vijay Sawlani
  6. Hajo Hamer
  7. Stephanie Gollwitzer
  8. Gernot Kreiselmeyer
  9. Marije J ter Wal
  10. Luca Kolibius
  11. Bernhard P Staresina
  12. Maria Wimber
  13. Matthew W Self
  14. Simon Hanslmayr
(2022)
Oscillations support short latency co-firing of neurons during human episodic memory formation
eLife 11:e78109.
https://doi.org/10.7554/eLife.78109

Share this article

https://doi.org/10.7554/eLife.78109

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