Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus
- Vanderbilt University, United States
- 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.
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Theta-and gamma-band oscillatory uncoupling in the macaque hippocampusZenodo, 10.5281/zenodo.7757458.
Article and author information
Author details
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
© 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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Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus
eLife 12:e86548.
https://doi.org/10.7554/eLife.86548
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
