The rate of transient beta frequency events predicts behavior across tasks and species

  1. Hyeyoung Shin  Is a corresponding author
  2. Robert Law
  3. Shawn Tsutsui
  4. Christopher I Moore
  5. Stephanie R Jones
  1. Brown University, United States
  2. Providence VA Medical Center, United States
15 figures and 1 additional file

Figures

Figure 1 with 1 supplement
Average 1 s prestimulus beta (15–29 Hz) power is higher on non-detected/attend out trials in SI.

(i) Mean prestimulus beta power as a function of time relative to stimulus onset in (A) human MEG during a tactile detection task (source localized data from hand area of SI; N = 10 subjects, 100 …

https://doi.org/10.7554/eLife.29086.002
Figure 1—figure supplement 1
Evoked response to suprathreshold sensory input and beta power on catch trials.

(A) (i) Human MEG evoked response to a suprathreshold tap to the fingertip of the third digit of the right hand. (reproduced from Jones et al., 2007) (ii) Mouse LFP evoked response to a …

https://doi.org/10.7554/eLife.29086.003
Beta emerges as brief events in non-averaged spectrograms.

(A) Top panel shows averaged spectrogram (1–40 Hz) in the 1 s prestimulus period from 100 trials, from an example subject in the human detection dataset (average across 100 non-detected trials). The …

https://doi.org/10.7554/eLife.29086.004
Schematic illustration of possible features underlying differences in averaged prestimulus beta power.

Given that surges in beta power in non-averaged data occur as transient events, higher trial mean beta power could be due to an increase in (A) event number (i.e. rate), (B) event power, (C) event …

https://doi.org/10.7554/eLife.29086.005
Beta events defined by a 6X median power cutoff show consistently high correlation with average prestimulus beta.

(i) Pearson’s correlation coefficient between mean prestimulus beta power and the percent area (i.e. percentage of pixels in the spectrogram) above cutoff in the non-averaged spectrogram, for …

https://doi.org/10.7554/eLife.29086.006
Figure 5 with 1 supplement
Beta event features are highly conserved across tasks and species.

Probability histogram for each prestimulus beta event feature; (i) event number, (ii) event power, (iii) event duration, (iv) event frequency span; defined at 6X median cutoff in each dataset (A–C). …

https://doi.org/10.7554/eLife.29086.007
Figure 5—figure supplement 1
Beta event duration and frequency span is stereotyped when maxima power is higher than 6X median cutoff.

Scatter plots of all local maxima aggregated across all subjects/sessions in each dataset.

https://doi.org/10.7554/eLife.29086.008
Figure 6 with 2 supplements
The number of beta events has a higher correlation with trial mean prestimulus beta power than event power, duration or frequency span.

Box and whisker plots over subjects/sessions depicting the Pearson’s correlation coefficients (R) between the trial summary of each beta event feature and trial mean prestimulus beta power. Note, …

https://doi.org/10.7554/eLife.29086.009
Figure 6—figure supplement 1
Example scatter plots showing relationship between trial mean prestimulus beta power and corresponding beta event number, trial mean event power, duration and frequency span.

Scatter plot showing trial-by-trial relationship between trial mean prestimulus beta power and trial summary of each event feature. Data shown for one representative subject (A, C)/session (B) from …

https://doi.org/10.7554/eLife.29086.010
Figure 6—figure supplement 2
Dependence of correlation with mean power on choice of cutoff.

Pearson’s correlation with trial mean prestimulus power for event number per trial (blue), trial mean event power (red), trial mean event duration (yellow) and trial mean event frequency span …

https://doi.org/10.7554/eLife.29086.011
Figure 7 with 2 supplements
Beta event number per trial (i.e. rate) consistently predicts detection/attention across tasks and species.

(i) Probability time histogram of beta event occurrence in the 1 s prestimulus window. Data binned in 50 ms windows, sliding in 1 ms steps. All other notations are same as Figure 1i. (ii-iv) …

https://doi.org/10.7554/eLife.29086.012
Figure 7—figure supplement 1
Dependence of relationship between beta event features and behavior on choice of power cutoff.

Percentage of subjects with DP/AP significantly less than 0.5 (i.e. beta is miss predictive) for trial summary of each beta event feature, over a range of cutoffs (significance determined by 95% …

https://doi.org/10.7554/eLife.29086.013
Figure 7—figure supplement 2
Optimal criterion for classifying behavior based on event number is two events per trial.

A-C (i) Probability histogram of event number across conditions (blue: detected/attend in; red: non-detected/attend out; mean ± SEM across subjects/sessions). (ii) % subjects/sessions with optimal …

https://doi.org/10.7554/eLife.29086.014
Figure 8 with 1 supplement
Non-detected trials are more likely to have a beta event closer to the time of the stimulus.

For each trial, the event occuring closest to the stimulus onset was termed the ‘most recent beta event’. All analyses are analogous to Figure 7, in the human (A) and mouse (B) detection datasets, …

https://doi.org/10.7554/eLife.29086.015
Figure 8—figure supplement 1
Dependence of relationship between ‘most recent beta event’ features and behavior on choice of cutoff.

Same as in Figure 7—figure supplement 1, but for ‘most recent beta event’ features.

https://doi.org/10.7554/eLife.29086.016
Independent influence of rate and timing on detection.

(i)Left panel: Event number histogram in detected (blue, mean ± SEM), non-detected (red, mean ± SEM), and event number matched (black, mean across subjects/sessions) trials via a random trial …

https://doi.org/10.7554/eLife.29086.017
Inter-event-interval (lEI) analyses suggest that beta events are not rhythmic or a renewal process.

(i) IEI distributions (20 ms bins) on detected/attend in (blue) and non-detected/attend out (red) conditions; mean across subjects with ± SEM as error bars. (ii) Fano factor and CV2 for each subject …

https://doi.org/10.7554/eLife.29086.018
Beta event findings are robust under redefinition of events as ‘non-overlapping beta events’.

(i) Probability histograms for number of local maxima per supra-cutoff region (i.e. a ‘non-overlapping beta event’), in detected (blue) and non-detected (red) trials; mean ± SEM across subjects. …

https://doi.org/10.7554/eLife.29086.019
Beta event emergence is consistent with a bursty generator mechanisms, as opposed to dynamic amplitude modulation of a sustained beta oscillation.

(A) Schematic illustration of two alternative mechanisms that could underlie transient surges in beta power in the spectrogram: (i) Dynamic Amplitude Modulation mechanism; versus, (ii) Bursty …

https://doi.org/10.7554/eLife.29086.020
Author response image 1
Hilbert-transformed amplitude histograms do not consistently show bimodality.

Hilbert-transformed amplitude histograms of band-pass (14~29Hz) filtered data for each subject / session in A. Human Detection, B. Mouse Detection, C. Human Attention datasets. The amplitude values …

Author response image 2
Spearman’s correlation with trial mean prestimulus beta power.

All trials were included for all features, and trial mean event power, duration and frequency span as zero for zero event trials.

Author response image 3
Multiple linear regression slopes, with trial mean prestimulus beta power as the response variable and the four trial summary event features as regressors.

All trials were included for all four features; trial mean event power, duration and frequency span were defined as zero for zero event trials.

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