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.

Dynamic Functional Connectivity of Emotion Processing in Beta Band with Naturalistic Emotion Stimuli

“…Another study reported activity in frontal electrodes during the emotional processing of IAPS pictures [ 83 , 84 ]. The conscious perception of visceral activity is generally reported in the right hemispheric part of the Insula [ 85 ] that contributes in the experience of emotions in the beta band [ 86 ]. Marshall et al [ 84 ] reported activity in frontal, frontocentral and frontotemporal electrodes in top-down anticipation of the heartbeat signal with increased sensory perception in the context of emotionally negative and neutral faces.…”

How can we detect and analyze traveling waves in human brain oscillations?

“…Our method overcomes these challenges by customizing the analysis pipeline according to the iEEG recordings from each individual patient (15,43). This approach consists of two primary steps: (i) The first step consists of identification of spatially contiguous clusters of electrodes with narrowband oscillations at similar frequencies.…”

“…Therefore, our first step in identifying these patterns is to detect oscillations that appear at a single frequency at multiple nearby electrodes. To detect such patterns, we first identify spatially contiguous clusters of electrodes with oscillations at the same or similar frequencies (15,43). Critically, we perform this procedure in an adaptive fashion that is well suited for human iEEG data by accommodating differences in electrode positions and oscillation frequencies across individuals.…”

“…We identify narrowband peaks in the normalized power spectrum as any local maximum greater than some predefined threshold. In our work (43), we used a threshold of one standard deviation above the mean, but other thresholds could be used depending on the experimenter's needs. This method reliably identifies the frequencies where individual electrodes show strong oscillations, as can be seen in Figure 2A.1 which shows our approach from two example electrodes.…”

“…Whereas the original electrode positions are of course in 3D in the brain's volumetric coordinates, we reduced the data to 2-D coordinates xi and yi corresponding to the cortical surface by projecting the 3-D Talairach coordinates of electrodes into the best-fitting 2-D plane using principal component analysis. Even though this procedure is most applicable to subdural grid electrodes, it can be applied to stereo EEG depth electrodes as well (43). This procedure can also be carried out in the 3-D volumetric space in the brain, however, projecting the 3-D coordinates to 2-D helps in better visualizing and interpreting the traveling wave (43).…”