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.
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.
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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We present near-atomic-resolution cryoEM structures of the mammalian voltage-gated potassium channel Kv1.2 in open, C-type inactivated, toxin-blocked and sodium-bound states at 3.2 Å, 2.5 Å, 3.2 Å, and 2.9 Å. These structures, all obtained at nominally zero membrane potential in detergent micelles, reveal distinct ion-occupancy patterns in the selectivity filter. The first two structures are very similar to those reported in the related Shaker channel and the much-studied Kv1.2–2.1 chimeric channel. On the other hand, two new structures show unexpected patterns of ion occupancy. First, the toxin α-Dendrotoxin, like Charybdotoxin, is seen to attach to the negatively-charged channel outer mouth, and a lysine residue penetrates into the selectivity filter, with the terminal amine coordinated by carbonyls, partially disrupting the outermost ion-binding site. In the remainder of the filter two densities of bound ions are observed, rather than three as observed with other toxin-blocked Kv channels. Second, a structure of Kv1.2 in Na+ solution does not show collapse or destabilization of the selectivity filter, but instead shows an intact selectivity filter with ion density in each binding site. We also attempted to image the C-type inactivated Kv1.2 W366F channel in Na+ solution, but the protein conformation was seen to be highly variable and only a low-resolution structure could be obtained. These findings present new insights into the stability of the selectivity filter and the mechanism of toxin block of this intensively studied, voltage-gated potassium channel.
