Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus

  1. Saman Abbaspoor
  2. Ahmed T Hussin
  3. Kari L Hoffman  Is a corresponding author
  1. Vanderbilt University, United States
  2. York University, Canada

Abstract

Nested hippocampal oscillations in the rodent give rise to temporal dynamics that may underlie learning, memory, and decision making. Although theta/gamma coupling in rodent CA1 occurs during exploration and sharp-wave ripples emerge in quiescence, it is less clear that these oscillatory regimes extend to primates. We therefore sought to identify correspondences in frequency bands, nesting, and behavioral coupling of oscillations taken from macaque hippocampus. We found that, in contrast to rodent oscillations, theta and gamma frequency bands in macaque CA1 were segregated by behavioral states. In both stationary and freely-moving designs, beta2/gamma (15-70 Hz) had greater power during visual search whereas the theta band (3-10 Hz; peak ~8 Hz) dominated during quiescence and early sleep. Moreover, theta band amplitude was strongest when beta2/slow gamma (20-35 Hz) amplitude was weakest, instead occurring along with higher frequencies (60-150 Hz). Spike-field coherence was most frequently seen in these three bands, (3-10 Hz, 20-35 Hz and 60-150 Hz); however, the theta-band coherence was largely due to spurious coupling during sharp-wave ripples. Accordingly, no intrinsic theta spiking rhythmicity was apparent. These results support a role for beta2/slow gamma modulation in CA1 during active exploration in the primate that is decoupled from theta oscillations. The apparent difference to the rodent oscillatory canon calls for a shift in focus of frequency when considering the primate hippocampus.

Data availability

The code used to process these data are available at https://github.com/hoffman-lab/Manuscripts/tree/main/AbbaspoorHussinHoffman2023. Data structures can be downloaded at https://zenodo.org/record/7757458. Previous reports from the stationary data are Leonard et al., 2015, Leonard et al., 2017, and Hussin et al., 2020.

The following data sets were generated

Article and author information

Author details

  1. Saman Abbaspoor

    Department of Psychology, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ahmed T Hussin

    Department of Biology, York University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Kari L Hoffman

    Department of Psychology, Vanderbilt University, Nashville, United States
    For correspondence
    kari.hoffman@vanderbilt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0560-8157

Funding

National Institutes of Neurological Disorders and Stroke (R01NS127128)

  • Saman Abbaspoor
  • Kari L Hoffman

Whitehall Foundation

  • Kari L Hoffman

Alzheimer's Society of Canada Doctoral Award

  • Ahmed T Hussin

National Science and Engineering Research Council (Discovery Grant)

  • Ahmed T Hussin
  • Kari L Hoffman

NSERC CREATE Vision Science and Applications

  • Ahmed T Hussin
  • Kari L Hoffman

Brain Canada Multi-Investigator Research Initiative

  • Ahmed T Hussin
  • Kari L Hoffman

The Krembil Foundation

  • Ahmed T Hussin
  • Kari L Hoffman

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

Reviewing Editor

  1. Martin Vinck, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the procedures were in accordance with a protocol approved by the local governing authorities. In the US this was the institutional animal care and use committee (IACUC # M1700152), and in Canada, this was the Canadian Council on Animal Care, local Animal Care Committee at York University (#2014-9).

Version history

  1. Preprint posted: January 1, 2022 (view preprint)
  2. Received: January 31, 2023
  3. Accepted: March 13, 2023
  4. Accepted Manuscript published: May 4, 2023 (version 1)
  5. Version of Record published: May 24, 2023 (version 2)

Copyright

© 2023, Abbaspoor 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. Saman Abbaspoor
  2. Ahmed T Hussin
  3. Kari L Hoffman
(2023)
Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus
eLife 12:e86548.
https://doi.org/10.7554/eLife.86548

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https://doi.org/10.7554/eLife.86548

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