Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
- Columbia University, United States
- Baylor College of Medicine, United States
- Thomas Jefferson University, United States
Abstract
The insula plays a fundamental role in a wide range of adaptive human behaviors, but its electrophysiological dynamics are poorly understood. Here we used human intracranial electroencephalographic recordings to investigate the electrophysiological properties and hierarchical organization of spontaneous neuronal oscillations within the insula. We analyzed the neuronal oscillations of the insula directly and found that rhythms in the theta and beta frequency oscillations are widespread and spontaneously present. These oscillations are largely organized along the anterior–posterior axis of the insula. Both the left and right insula showed anterior-to-posterior decreasing gradients for the power of oscillations in the beta frequency band. The left insula also showed a posterior-to-anterior decreasing frequency gradient and an anterior-to-posterior decreasing power gradient in the theta frequency band. In addition to measuring the power of these oscillations, we also examined the phase of these signals across simultaneous recording channels and found that the insula oscillations in the theta and beta bands are traveling waves. The strength of the traveling waves in each frequency was positively correlated with the amplitude of each oscillation. However, the theta and beta traveling waves were uncoupled to each other in terms of phase and amplitude, which suggested that insular traveling waves in the theta and beta bands operate independently. Our findings provide new insights into the spatiotemporal dynamics and hierarchical organization of neuronal oscillations within the insula, which, given its rich connectivity with widespread cortical regions, indicates that oscillations and traveling waves have an important role in intra- and inter-insular communication.
Data availability
Deidentified data are fully available to the public without any restrictions and can be downloaded here https://dabi.loni.usc.edu/dsi/anon?token=Do2yMlnZiXwKwFmOeCDtK. Codes used for the analyses are also fully available to the public without any restrictions and can be downloaded here https://github.com/john-myers-github/INSULA_RS.
Article and author information
Author details
Funding
National Institutes of Health (R01-MH127006)
- Brian A Metzger
- Kelly Bijanki
National Institutes of Health (K01-MH116364)
- Brian A Metzger
- Kelly Bijanki
National Science Foundation (CAREER Award)
- Joshua Jacobs
McNair Foundation (McNair Foundation)
- Sameer A Sheth
Dana Foundation (Dana Foundation)
- Sameer A Sheth
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Shella Keilholz, Emory University and Georgia Institute of Technology, United States
Ethics
Human subjects: All decisions regarding the location and coverage of the iEEG probes were based solely on clinical criteria. The Baylor College of Medicine Institutional Review Board approved placement of all electrodes (IRB-18112). All patients provided informed consent before participating.
Version history
- Preprint posted: December 19, 2021 (view preprint)
- Received: December 29, 2021
- Accepted: May 25, 2022
- Accepted Manuscript published: May 26, 2022 (version 1)
- Version of Record published: June 15, 2022 (version 2)
Copyright
© 2022, Das 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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Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
eLife 11:e76702.
https://doi.org/10.7554/eLife.76702
Further reading
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Asymmetries in the size of structures deep below the cortex explain how alpha oscillations in the brain respond to shifts in attention.
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Evidence suggests that subcortical structures play a role in high-level cognitive functions such as the allocation of spatial attention. While there is abundant evidence in humans for posterior alpha band oscillations being modulated by spatial attention, little is known about how subcortical regions contribute to these oscillatory modulations, particularly under varying conditions of cognitive challenge. In this study, we combined MEG and structural MRI data to investigate the role of subcortical structures in controlling the allocation of attentional resources by employing a cued spatial attention paradigm with varying levels of perceptual load. We asked whether hemispheric lateralization of volumetric measures of the thalamus and basal ganglia predicted the hemispheric modulation of alpha-band power. Lateral asymmetry of the globus pallidus, caudate nucleus, and thalamus predicted attention-related modulations of posterior alpha oscillations. When the perceptual load was applied to the target and the distractor was salient caudate nucleus asymmetry predicted alpha-band modulations. Globus pallidus was predictive of alpha-band modulations when either the target had a high load, or the distractor was salient, but not both. Finally, the asymmetry of the thalamus predicted alpha band modulation when neither component of the task was perceptually demanding. In addition to delivering new insight into the subcortical circuity controlling alpha oscillations with spatial attention, our finding might also have clinical applications. We provide a framework that could be followed for detecting how structural changes in subcortical regions that are associated with neurological disorders can be reflected in the modulation of oscillatory brain activity.
