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

Abstract
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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

1. Abbaspoor S
2. et al
(2023) Theta-and gamma-band oscillatory uncoupling in the macaque hippocampus
Zenodo, 10.5281/zenodo.7757458.

https://zenodo.org/record/7757458

Article and author information

Author details

Saman Abbaspoor

Department of Psychology, Vanderbilt University, Nashville, United States

Competing interests
The authors declare that no competing interests exist.
Ahmed T Hussin

Department of Biology, York University, Toronto, Canada

Competing interests
The authors declare that no competing interests exist.
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.

"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.

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).

Copyright

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.