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• W2895955185 abstract "Oscillatory activity in the brain has a long tradition of study, with Hans Berger, the founder of electroencephalography, immediately noting its significance.1 Such oscillatory activity is most commonly measured by examining the frequency content of potentials recorded from an electrode in or near the cerebral cortex. These potentials are thought to represent summated synaptic potentials from the cortex closest to the electrode.2 While the temporal properties of oscillatory activity recorded from single electrodes have been extensively studied, spatial properties have gained more attention recently with the increased prevalence of recording brain signals with multiple, spatially distributed sensors (like the grids and strips of electrodes used in epilepsy surgery).3 That distributed oscillations are important is widely accepted, for instance in the well-described waves of sleep and epilepsy. But why oscillations are distributed remains unknown. Are areas using the oscillations to communicate, like a handshake, or do the waves travel from one area to another like ripples on a pond. In support of the latter interpretation, that of traveling waves, Zhang et al4 recently followed up on their previous work reporting traveling theta waves along the long axis of the human hippocampus.5 While several other studies have shown traveling waves in local neural signals,6 their study is the first to relate large-scale cortical traveling wave features to memory task behavior in a large group of human subjects. In their paper, the authors examined traveling waves across the neocortex of a large cohort of 77 epilepsy patients who were performing a Sternberg-like memory task.7 The authors first discovered spatially contiguous groups of electrodes with the same oscillatory frequencies ranging from 2 to 15 Hz, and then looked for systematic delays in the phases of these oscillations among electrodes in each group. They discovered systematic delays that exceeded a statistical threshold in 67% of the electrode groups, thereby concluding that theta and alpha oscillations are traveling waves that span a broad area of the cerebral cortex. The traveling waves that Zhang et al4 found had some interesting features that correlate with previously reported oscillatory frequencies.8,9 Waves in different lobes exhibited different carrier frequencies with frontal waves occurring more in the theta range, and occipital, parietal, and temporal waves occurring more in the alpha range. Traveling wave directions also differed among lobes. Traveling waves in the temporal and frontal lobes appeared to propagate from posterior to anterior, though traveling waves from the parietal and occipital lobes did not exhibit a consistent propagation direction. These direction and frequency results were beautifully depicted in Figure 24 by the video game designer in the Jacobs Lab, Ansh Patel. Zhang et al4 further examine the relationships among features of cortical traveling waves and the behavior of the subjects in which they were observed. They did this by examining the consistency among traveling wave directions through the duration of trials in the memory task. The authors found that traveling waves in parietal and occipital electrodes had more consistent directions earlier during a trial of the memory task, whereas frontal and temporal electrodes had more consistent directions later during a trial of the memory task. Moreover, the degree of consistency correlated with performance. While these trends in directional consistency were significant, the overall changes in consistency through the trial durations were approximately 2% in size. Across trials and subjects, the directional consistency was approximately 15% on average. These small effect sizes are compounded by the fact that the results do not account for random variance that might occur across subjects or behavioral sessions, as could be accomplished with linear mixed effects models, rather than pooling results across patients and testing hypotheses with analysis of variance. Finally, Zhang et al4 posit that the traveling wave features observed in human theta and alpha oscillations are best explained by a weakly coupled oscillator model. One of the predictions of this model is that waves travel along the gradient of oscillation frequency, from fast oscillations to slower ones, which is exactly what was observed in their population of patients. However, the assumptions for the weakly coupled oscillator model make it difficult to square with existing data on the propagation speeds of other traveling waves. While Zhang et al4 report a significant, positive correlation between oscillation frequency and traveling wave speed, other studies measuring traveling wave speeds on microelectrode arrays report speeds that differ markedly. The mean reported speed from Zhang et al4 is 0.55 m/s that is slightly faster than traveling waves associated with the failure of surround inhibition during seizures,10 and about five times faster than seizure traveling waves in tissue in which inhibition is maintained.11,12 The wave speeds reported in Zhang et al4 are also slightly faster than those observed in beta-range local field potentials in macaque and cat visual cortices.13,14 This discrepancy is notable, as a fundamental assumption of the authors’ coupled oscillator explanation relies on the linear correlation between wave speed and oscillation frequency. Additionally, the authors’ previously reported traveling wave speeds along the long axis of the hippocampus are close to twice as fast as those reported in the current study.5 These discrepancies in speed estimation could reflect differing physiological properties that underlie traveling wave generation, or could reflect measurement biases from traveling wave estimation on different spatial scales. Alternatively, the weakly coupled oscillator model might only apply for some traveling waves and not others. In any case, the dynamics of traveling waves in the brain will likely be an interesting area of future study that could elucidate information processing pathways or hierarchies in the brain. These studies should focus on both how traveling wave features relate to behavior, and understanding discrepancies between traveling wave speeds measured on the micro- and mesoscale in order to inform mechanistic computational models of information flow in local and long-range cortical circuits. Disclosures John Rolston is supported by an NIH NCATS career development award (KL2TR002539). The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article." @default.
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• W2895955185 date "2018-10-15" @default.
• W2895955185 modified "2023-10-17" @default.
• W2895955185 title "Oscillations Travel Around the Human Brain" @default.
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• W2895955185 doi "https://doi.org/10.1093/neuros/nyy402" @default.
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