Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
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.
Metrics
-
- 3,125
- views
-
- 645
- downloads
-
- 24
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Humans make irrational decisions in the presence of irrelevant distractor options. There is little consensus on whether decision making is facilitated or impaired by the presence of a highly rewarding distractor, or whether the distractor effect operates at the level of options’ component attributes rather than at the level of their overall value. To reconcile different claims, we argue that it is important to consider the diversity of people’s styles of decision making and whether choice attributes are combined in an additive or multiplicative way. Employing a multi-laboratory dataset investigating the same experimental paradigm, we demonstrated that people used a mix of both approaches and the extent to which approach was used varied across individuals. Critically, we identified that this variability was correlated with the distractor effect during decision making. Individuals who tended to use a multiplicative approach to compute value, showed a positive distractor effect. In contrast, a negative distractor effect (divisive normalisation) was prominent in individuals tending towards an additive approach. Findings suggest that the distractor effect is related to how value is constructed, which in turn may be influenced by task and subject specificities. This concurs with recent behavioural and neuroscience findings that multiple distractor effects co-exist.
-
- Neuroscience
The subthalamic nucleus (STN) plays critical roles in the motor and cognitive function of the basal ganglia (BG), but the exact nature of these roles is not fully understood, especially in the context of decision-making based on uncertain evidence. Guided by theoretical predictions of specific STN contributions, we used single-unit recording and electrical microstimulation in the STN of healthy monkeys to assess its causal, computational roles in visual-saccadic decisions based on noisy evidence. The recordings identified subpopulations of STN neurons with distinct task-related activity patterns that related to different theoretically predicted functions. Microstimulation caused changes in behavioral choices and response times that reflected multiple contributions to an ‘accumulate-to-bound’-like decision process, including modulation of decision bounds and evidence accumulation, and to non-perceptual processes. These results provide new insights into the multiple ways that the STN can support higher brain function.