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The direction of theta and alpha travelling waves modulates human memory processing

Nature Human Behaviour (2024)Cite this article

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Abstract

To support a range of behaviours, the brain must flexibly coordinate neural activity across widespread brain regions. One potential mechanism for this coordination is a travelling wave, in which a neural oscillation propagates across the brain while organizing the order and timing of activity across regions. Although travelling waves are present across the brain in various species, their potential functional relevance has remained unknown. Here, using rare direct human brain recordings, we demonstrate a distinct functional role for travelling waves of theta- and alpha-band (2–13 Hz) oscillations in the cortex. Travelling waves propagate in different directions during separate cognitive processes. In episodic memory, travelling waves tended to propagate in a posterior-to-anterior direction during successful memory encoding and in an anterior-to-posterior direction during recall. Because travelling waves of oscillations correspond to local neuronal spiking, these patterns indicate that rhythmic pulses of activity move across the brain in different directions for separate behaviours. More broadly, our results suggest a fundamental role for travelling waves and oscillations in dynamically coordinating neural connectivity, by flexibly organizing the timing and directionality of network interactions across the cortex to support cognition and behaviour.

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Fig. 1: Example TW at 8.9 Hz in patient 34’s left hemisphere.
Fig. 2: Changes in TW direction across memory encoding and recall.
Fig. 3: Example participants where TWs varied in propagation direction with memory processing.
Fig. 4: Population analysis of TW direction shifts during memory encoding and recall.

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Data availability

The raw electrophysiological data used in this study are available upon request at https://memory.psych.upenn.edu/Data_Request.

Code availability

The custom code and analyses are available at https://github.com/umarmohan/freerecall_travelingwaves.

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Acknowledgements

We thank the patients for participating in our study. This work was supported by the DARPA Restoring Active Memory programme (Cooperative Agreement No. N66001-14-2-4032); National Institutes of Health Grant Nos R01-MH104606, U01-NS113198 and RF1-MH114276; and the National Science Foundation (to J.J.). The views, opinions and/or findings expressed are those of the authors and should not be interpreted as representing the official views or policies of the Department of Defense or the US government. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank J. Chapeton, A. Das, T. Donoghue, M. Hermiller, L. Kunz, S. Favila, J. Gottlieb, B. Lega, S. Qasim and E. Zabeh for providing helpful critical feedback on the manuscript. We thank M. Kahana, P. Wanda and J. Rudoler for providing data and technical support.

Author information

Authors and Affiliations

  1. Surgical Neurology Branch, NINDS, National Institutes of Health, Bethesda, MD, USA

    Uma R. Mohan

  2. Amazon Corporation, Seattle, WA, USA

    Honghui Zhang

  3. Department of Mathematics, University of Pittsburgh, Pittsburgh, PA, USA

    Bard Ermentrout

  4. Department of Biomedical Engineering, Columbia University, New York City, NY, USA

    Joshua Jacobs

  5. Department of Neurological Surgery, Columbia University, New York City, NY, USA

    Joshua Jacobs

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Contributions

U.R.M., H.Z., B.E. and J.J. designed and implemented the data analyses. U.R.M., B.E. and J.J. wrote the manuscript.

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Correspondence to Joshua Jacobs.

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Extended data

Extended Data Fig. 1 Exclusion of trials with potential inaccurate measurement of propagation direction due to spatial aliasing.

(A) Adequate spatial sampling when low-frequency oscillations propagate propagate across 3 widely spaced electrodes(left). Inadequate spatial sampling for higher-frequency oscillations propagating across 3 electrodes with the same spacing (middle). Arrows indicate two possible propagation direction measurements. Higher density electrode spacing would disambiguate the true propagation direction (right). (B) Combinations of oscillation frequencies and phase velocities where there is adequate and inadequate spatial sampling with 1 cm electrode spacing, determined by whether half the spatial wavelength of a propagating oscillation is less than 1 cm, shown in green and red, respectively. (C) Example 1 s of a trial with a traveling wave propagating in space across five adjacent electrodes of an alpha oscillation cluster in patient 34. (D) Time-lagged cross correlation for entire trial measured between adjacent electrodes (a) and (b) in oscillation cluster. Time of maximum coupling measured at -11 ms indicated by red star showing signal on electrode (b) leads electrode (a). (E) Correlation between time differences between electrodes (a) and (b) measured via phase differences with the time-lag measured from cross-correlation for unsuccessful encoding trial son the left and successful encoding trials on the right. Strong correlation along unity lines indicates alignment between the two measurements such that no trials were susceptible to spatial aliasing. (F) Correlation between phase-based time differences and correlation-based time differences for a beta oscillation cluster with 18% of trials showing an inconsistency between the two methods. Red time lags measured via cross-correlation indicate that the true lag between the signals on those trials was approximately a cycle forward or backwards indicating the potential for spatial aliasing when measuring only using phase. (G) When excluding trials with these inconsistencies across all clusters in the dataset, approximately 83% of trials were not susceptible to spatial aliasing (right) across all oscillation clusters (n=421). Error bars denote ± 1 SEM. (H) Percent of trials in which the correct direction could be measured using phase differences when perfect sinusoidal signals were shifted across five simulated electrodes (n=421). (I) Percent of trials in which the correct direction could be measured using phase differences when imperfect eeg signals were shifted across five simulated electrodes (n=421). (J) Percent of trials in which the correct direction could be measured using phase differences when real eeg signals were shifted across five simulated electrodes after excluding trials that were susceptible to spatial aliasing (n=421).

Extended Data Fig. 2 Narrowband power at oscillation clusters that showed traveling waves in the episodic memory task.

(A) Mean normalized narrowband power centered around each oscillation cluster’s peak frequency across all 93 participants, calculated with the log-transformed amplitude of the Hilbert transform prior to selecting trials with sufficient oscillatory power, wave strength, and no potential for spatial aliasing. (B) Mean normalized narrowband power for oscillation clusters that showed traveling waves averaged over time in all 93 participants, separately calculated during time periods when TWs moved posteriorly and anteriorly, during successful and unsuccessful encoding trials. There were no significant differences in mean power across the clusters that showed posterior and anterior propagation (all p’s > 0.05, two-sided t-test). Error bars denote ± 1 SEM.

Extended Data Fig. 3 Example data showing the absence of traveling waves.

(A) Example trial where a traveling wave was not present on a cluster that often showed 8.9-Hz oscillations that propagated as TWs on other trials. Filtered signals from five channels during one trial of memory task from participant 34. (B) Timecourse of adjusted τ2 across the cluster used to measure statistical reliability of circular-linear models fit to the phase gradients. (C) Brain map with arrows indicating, for each electrode, the calculated local propagation direction. Arrow color indicates relative phase at time indicated by black line in A. (D-F) Same as (A-C) for additional example trial.

Extended Data Fig. 4 Characteristics of cortical traveling waves during encoding and recall of episodic memory task.

(A) Histogram of the peak oscillation frequencies for clusters with TWs. All green histograms are properties measured during encoding and blue during recall. (B) Histogram of the number of electrodes in each cluster. (C) Histogram of the counts of clusters per patient that showed TWs. Most participants had 2 to 4 clusters across different sets of grid and strip electrodes or groups of electrodes with oscillations at different peak frequencies. A few patients had 5 or more. Patients with many clusters often had multiple smaller clusters of 5-6 electrodes in different regions and hemispheres. (D) Distribution of the percentage of single trials that show reliable TWs for individual clusters. (E) Histogram of TW propagation phase velocities across clusters. Black line indicates median. (F) Histogram of TW spatial wavelength.

Extended Data Fig. 5 Examples of clusters that showed traveling waves with different types of directional propagation patterns.

Plots show example direction distribution for TWs we labeled as propagating in (A) unidirectional, (B) bidirectional, and (C) nondirectional fashions.

Extended Data Fig. 6 Population categorization of cluster direction patterns in episodic memory task.

(A) Percent of TW clusters in each oscillatory range identified as bidirectional, unidirectional, and nondirectional across all 93 participants. (B) Mean percent recall rates across 93 participants that showed a TW cluster with unidirectional, bidirectional, and nondirectional TW propagation, by oscillatory frequency band (linear mixed effects model, bidirectional vs. unidirectional clusters: p=0.062; bidirectional vs. nondirectional TW clusters:, p=0.002, Tukey contrast multiple comparisons test). Error bars denote ± 1 SEM. (*p < 0.05, * * p < 0.01, two-sided t-test). Overall, participants who showed bidirectional TW propagation showed a 5.8% higher rate of successful memory encoding compared to participants with unidirectional and multidirectional patterns, indicating that bidirectional TW propagation may be a feature of normal cognition.

Extended Data Fig. 7 Traveling waves in example participants who showed a link between TW direction and memory.

(A) Example traveling wave in patient 89 at 7.8 Hz; format of individual plots follows Fig. 3. (B) Example traveling wave frontal cortex of patient 130 at 10.8 Hz.

Extended Data Fig. 8 Direction distributions during memory encoding and recall.

(A) Distribution of clusters’ pre-dominant propagation directions for all theta TWs measured on oscillation clusters in the Frontal, Temporal, and Parietal/Occipital regions during memory encoding and recall at the timepoint of maximal memory-related effects. TW propagation directions were weighted by the proportion of trials with TWs propagating in each directions captured (see Methods). (B) Same as (A) for alpha-band TWs (C) Same as (A) for beta-band TWs.

Extended Data Fig. 9 Relation between TW directional shifts and memory processing.

(A) Normalized difference in the prevalence of TWs propagating in the preferred encoding direction versus the opposite direction for successful encoding relative to the cluster’s natural bidirecitonal split (averaged across word presentation intervals). Asterisks indicate specific regions and oscillatory bands where the normalized percent of TWs traveling in preferred encoding directions across clusters is significantly above a distribution of shuffled TW directions (p’s < 0.05, one-sided binomial tests against 0, Cluster counts in Suplementary Table 1). Error bars denote ± 1 SEM. (B) Normalized difference of TWs propagating in preferred encoding versus preferred recall direction averaged during 2 seconds prior to verbal recall. Asterisks indicate specific regions and oscillatory bands where the normalized percent of TWs traveling in preferred encoding directions across clusters is significantly below a distribution of shuffled TW directions (p’s < 0.05, one-sided binomial tests).

Extended Data Fig. 10 Hypothesized relations between traveling wave (TW) direction and memory processes.

When presented with a list of words during an episodic memory task, successful memory encoding more likely when waves propagated in the preferred encoding direction, as opposed to the opposite direction, characterized as the preferred recall direction. We hypothesize that preferred encoding and preferred recall TW propagation may reflect more general neural processes including feedforward and feedbackward cortical processing, respectively.

Supplementary information

Supplementary Information

Supplementary Tables 1–3, Figs. 1–3 and captions for Supplementary Videos 1 and 2.

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Supplementary Video 1

Example animation of a TW in patient 34 on a trial where memory encoding was successful (related to Fig. 2). The animation includes filtered signals during the trial, local propagation directions indicated on the brain map, a single arrow of mean direction across electrodes and the topography of TW phase over time. A single arrow indicating the mean direction across electrodes is visible when the wave is reliable.

Supplementary Video 2

Example TW on a trial where memory encoding was unsuccessful. The data are from patient 34. The video is in the same format as Supplementary Video 1.

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Mohan, U.R., Zhang, H., Ermentrout, B. et al. The direction of theta and alpha travelling waves modulates human memory processing. Nat Hum Behav (2024). https://doi.org/10.1038/s41562-024-01838-3

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