Ripples reflect a spectrum of synchronous spiking activity in human anterior temporal lobe

  1. Ai Phuong S Tong
  2. Alex P Vaz
  3. John H Wittig Jr.
  4. Sara K Inati
  5. Kareem A Zaghloul  Is a corresponding author
  1. National Institute of Neurological Disorders and Stroke, National Institutes of Health, United States
  2. Duke University School of Medicine, United States

Abstract

Direct brain recordings have provided important insights into how high frequency activity captured through intracranial EEG (iEEG) supports human memory retrieval. The extent to which such activity is comprised of transient fluctuations that reflect the dynamic coordination of underlying neurons, however, remains unclear. Here, we simultaneously record iEEG, local field potential (LFP), and single unit activity in the human temporal cortex. We demonstrate that fast oscillations within the previously identified 80-120 Hz ripple band contribute to 70-200 Hz high frequency activity in the human cortex. These ripple oscillations exhibit a spectrum of amplitudes and durations related to the amount of underlying neuronal spiking. Ripples in the macro-scale iEEG are related to the number and synchrony of ripples in the micro-scale LFP, which in turn are related to the synchrony of neuronal spiking. Our data suggest that neural activity in the human temporal lobe is organized into transient bouts of ripple oscillations that reflect underlying bursts of spiking activity.

Data availability

Data and custom code used in this study can be found at https://neuroscience.nih.gov/zaghloul/downloads.html. Source code and data files have been uploaded for Figures 1-4.

Article and author information

Author details

  1. Ai Phuong S Tong

    Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Alex P Vaz

    Medical Scientist Training Program, Duke University School of Medicine, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. John H Wittig Jr.

    Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0465-1022
  4. Sara K Inati

    Office of the Clinical Director, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Kareem A Zaghloul

    Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States
    For correspondence
    kareem.zaghloul@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8575-3578

Funding

NINDS grant F31 NS113400

  • Alex P Vaz

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

Ethics

Human subjects: Data were collected at the Clinical Center at the National Institutes of Health (NIH; Bethesda, MD). The Institutional Review Board (IRB) approved the research protocol (11-N-0051), and informed consent was obtained from the participants and their guardians.

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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https://doi.org/10.7554/eLife.68401

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