1. Neuroscience

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
https://doi.org/10.7554/eLife.32554
Share this article
Cite this article
  1. Andrew J Watrous
  2. Jonathan Miller
  3. Salman E Qasim
  4. Itzhak Fried
  5. Joshua Jacobs
(2018)
Phase-tuned neuronal firing encodes human contextual representations for navigational goals
eLife 7:e32554.
https://doi.org/10.7554/eLife.32554
  2. Download BibTeX
  3. Download .RIS

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.

Data availability

The human single neuron recordings raw data can be obtained upon request from Joshua Jacobs (joshua.jacobs@columbia.edu). At this point, the raw data has not been made publicly available to ensure controlled access to the dataset and that the patients' anonymity is not compromised.

The following previously published data sets were used

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.

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

  • 3,204
    views
  • 466
    downloads
  • 95
    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. Andrew J Watrous
  2. Jonathan Miller
  3. Salman E Qasim
  4. Itzhak Fried
  5. Joshua Jacobs
(2018)
Phase-tuned neuronal firing encodes human contextual representations for navigational goals
eLife 7:e32554.
https://doi.org/10.7554/eLife.32554

Share this article

https://doi.org/10.7554/eLife.32554

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Phase-amplitude coupling supports phase coding in human ECoG

    Andrew J Watrous, Lorena Deuker ... Nikolai Axmacher
    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. Neuroscience

    Metabolism: Insulin control in fruit flies

    Omowumi Kayode
    Insight

    Investigating how the production of insulin is regulated in fruit flies reveals surprising insights that may help to better understand how this process unfolds in humans.

    1. Neuroscience

    Unraveling the impact of congenital deafness on individual brain organization

    Lenia Amaral, Xiaosha Wang ... Ella Striem-Amit
    Research Article

    Research on brain plasticity, particularly in the context of deafness, consistently emphasizes the reorganization of the auditory cortex. But to what extent do all individuals with deafness show the same level of reorganization? To address this question, we examined the individual differences in functional connectivity (FC) from the deprived auditory cortex. Our findings demonstrate remarkable differentiation between individuals deriving from the absence of shared auditory experiences, resulting in heightened FC variability among deaf individuals, compared to more consistent FC in the hearing group. Notably, connectivity to language regions becomes more diverse across individuals with deafness. This does not stem from delayed language acquisition; it is found in deaf native signers, who are exposed to natural language since birth. However, comparing FC diversity between deaf native signers and deaf delayed signers, who were deprived of language in early development, we show that language experience also impacts individual differences, although to a more moderate extent. Overall, our research points out the intricate interplay between brain plasticity and individual differences, shedding light on the diverse ways reorganization manifests among individuals. It joins findings of increased connectivity diversity in blindness and highlights the importance of considering individual differences in personalized rehabilitation for sensory loss.