1. Neuroscience
Download icon

Phase-tuned neuronal firing encodes human contextual representations for navigational goals

  1. Andrew J Watrous  Is a corresponding author
  2. Jonathan Miller
  3. Salman E Qasim
  4. Itzhak Fried
  5. Joshua Jacobs
  1. Columbia University, United States
  2. University of California, Los Angeles, United States
Research Advance
  • Cited 17
  • Views 1,962
  • Annotations
Cite this article as: eLife 2018;7:e32554 doi: 10.7554/eLife.32554

Abstract

We previously demonstrated that the phase of oscillations modulates neural activity representing categorical information using human intracranial recordings and high-frequency activity from local field potentials (Watrous et al., 2015b). We extend these findings here using human single-neuron recordings during a navigation task. We identify neurons in the medial temporal lobe with firing-rate modulations for specific navigational goals, as well as for navigational planning and goal arrival. Going beyond this work, using a novel oscillation detection algorithm, we identify phase-locked neural firing that encodes information about a person's prospective navigational goal in the absence of firing rate changes. These results provide evidence for navigational planning and contextual accounts of human MTL function at the single-neuron level. More generally, our findings identify phase-coded neuronal firing as a component of the human neural code.

Article and author information

Author details

  1. Andrew J Watrous

    Department of Biomedical Engineering, Columbia University, New York, United States
    For correspondence
    andrew.j.watrous@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3107-3726

  2. Jonathan Miller

    Department of Biomedical Engineering, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Salman E Qasim

    Department of Biomedical Engineering, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Itzhak Fried

    Department of Neurosurgery, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5962-2678

  5. Joshua Jacobs

    Department of Biomedical Engineering, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Neurological Disorders and Stroke (NS033221)

  • Itzhak Fried

National Institute of Neurological Disorders and Stroke (NS084017)

  • Itzhak Fried

National Institute of Mental Health (MH104606)

  • Joshua Jacobs

National Science Foundation (DGE 16-44869)

  • Salman E Qasim

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

Ethics

Human subjects: The Medical Institutional Review Board at the University of California-Los Angeles approved this study (IRB#10-000973) involving recordings from patients with drug-resistant epilepsy who provided informed consent to participate in research.

Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Publication history

  1. Received: October 12, 2017
  2. Accepted: June 21, 2018
  3. Accepted Manuscript published: June 22, 2018 (version 1)
  4. Version of Record published: July 11, 2018 (version 2)

Copyright

© 2018, Watrous 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

  • 1,962
    Page views
  • 329
    Downloads
  • 17
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, 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)

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

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

Categories and tags

Research organism

    1. Builds upon

    Phase-amplitude coupling supports phase coding in human ECoG

    Andrew J Watrous et al.
  2. Further reading

Further reading

    1. Neuroscience

    Phase-amplitude coupling supports phase coding in human ECoG

    Andrew J Watrous et al.
    Research Article Updated

    Prior studies have shown that high-frequency activity (HFA) is modulated by the phase of low-frequency activity. This phenomenon of phase-amplitude coupling (PAC) is often interpreted as reflecting phase coding of neural representations, although evidence for this link is still lacking in humans. Here, we show that PAC indeed supports phase-dependent stimulus representations for categories. Six patients with medication-resistant epilepsy viewed images of faces, tools, houses, and scenes during simultaneous acquisition of intracranial recordings. Analyzing 167 electrodes, we observed PAC at 43% of electrodes. Further inspection of PAC revealed that category specific HFA modulations occurred at different phases and frequencies of the underlying low-frequency rhythm, permitting decoding of categorical information using the phase at which HFA events occurred. These results provide evidence for categorical phase-coded neural representations and are the first to show that PAC coincides with phase-dependent coding in the human brain.

    1. Biochemistry and Chemical Biology
    2. Neuroscience

    Science Forum: Addressing selective reporting of experiments through predefined exclusion criteria

    Kleber Neves, Olavo B Amaral
    Feature Article
    1. Human Biology and Medicine
    2. Neuroscience

    Aberrant subchondral osteoblastic metabolism modifies NaV1.8 for osteoarthritis

    Jianxi Zhu et al.
    Research Article