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Articles, Behavioral/Cognitive

Neural Microstates Govern Perception of Auditory Input without Rhythmic Structure

Molly J. Henry, Björn Herrmann and Jonas Obleser
Journal of Neuroscience 20 January 2016, 36 (3) 860-871; DOI: https://doi.org/10.1523/JNEUROSCI.2191-15.2016
Molly J. Henry
1Max Planck “Auditory Cognition” Research Group, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany and
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Björn Herrmann
1Max Planck “Auditory Cognition” Research Group, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany and
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Jonas Obleser
1Max Planck “Auditory Cognition” Research Group, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany and
2Department of Psychology, University of Lübeck, 23562 Lübeck, Germany
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    Figure 1.

    a, Acoustic stimulus structure. Top, Stimuli were narrow-band noises without low-frequency rhythmic structure. Hilbert envelope is overlaid in green. Two, three, or four gaps (marked by arrows) were embedded in each 14 s stimulus. Bottom, Frequency-domain representation of acoustic stimuli for a single representative participant; amplitude spectra for individual stimuli are shown in gray, and the average over stimuli is overlaid in green. Inset, Average amplitude spectrum up to 100 Hz. b, Frequency-domain neural responses. Top, Autopower (left, both oscillatory and 1/fβ contributions) and cross-power (right, 1/fβ contributions only) spectral densities calculated for coarse-graining spectral analysis, plotted in log–log coordinates for single participants (green, gray) with the mean overlaid (black, thick line). Fits from which power-law exponents, β, were estimated for low (0.1–8 Hz) and high (12–100 Hz) frequencies are overlaid in pink. Subtracting cross-power spectral density from autopower spectral density yields an estimate of the oscillatory contributions to power (inset, left). Oscillatory power was significantly nonzero at all frequency bins between 3.4 and 10.75 Hz (marked by gray bar). Power-law exponents, β, differed significantly between auto- and cross-power spectral densities for both low (p < 0.001) and high (p = 0.003) frequencies (inset, right). Topographies are shown below for the classically defined delta (1–4 Hz), theta (4–8 Hz), and alpha (8–12 Hz) frequency bands in the autopower spectral density function.

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    Figure 2.

    a, Correlation between neural phase and hit rate. Z-scored circular–linear correlations between binned gap-detection hit rates and neural phase for frequencies ranging between 1 and 15 Hz and for −0.5 to 0 s before gap, plotted for electrode Cz. Significant clusters (outlined in black) were observed in the delta (1–2.5 Hz, −0.50 to 0 s), theta (5–6.5 Hz, −0.24 to −0.20 s), low-alpha (8–12 Hz, −0.23 to −0.16 s), and high-alpha (9–15 Hz; −0.03 to 0 s) frequency bands. b, Single-participant data in significant clusters. Left, Nonaligned, zero-centered binned hit rates plotted as a function of neural phase in the significant delta (1–2.5 Hz), theta (5–6.5 Hz), low-alpha (8–12 Hz), and high-alpha (9–15 Hz) clusters; single-participant hit rates are shown in gray, and grand-average hit rates are overlaid in black. Middle, Analysis of optimal neural phase (i.e., the neural phase in which hit rate was highest) in each frequency band revealed that neural phase effects were only consistent across participants in the delta frequency band (delta, pFDR = 0.048; all other pFDR ≥ 0.30). Right, Zero-centered binned hit rates plotted as a function of neural phase. Single-participant data were realigned so that maximum hit rates for each participant coincided (arbitrarily aligned with peak hit rate at phase = 0 rad); single-participant hit rates are shown in gray, and grand-average hit rates are overlaid in black.

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    Figure 3.

    Delta phase mediated the influence of high-alpha phase on gap-detection hit rates. Hit rates (zero centered) are shown as a function of high-alpha (9–15 Hz) neural phase, separately for each of four delta phase bins (illustrated at bottom of figure). Single-participant data are shown in gray, and grand-average data are overlaid in black (thick lines). Circle plots show distributions of optimal neural phases estimated from cosine fits with resultant vectors. High-alpha (9–15 Hz) phase had a consistent influence on gap-detection hit rates only when delta (1–2.5 Hz) phase ranged between π/4 and –3π/4 (encompassing 0; far right).

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    Figure 4.

    Delta phase mediated the joint influence of theta and low-alpha phase on gap-detection hit rates. Hit rates are plotted on tori as a function of 5–6.5 Hz theta phase (smaller, inside circle) and 8–12 Hz low-alpha phase (larger, outside circle), separately for each of four delta phase bins (illustrated at bottom of figure). Theta and low-alpha phase marginally significantly comodulated hit rates only for trials on which delta phase ranged between 3π/4 and –π/4 (encompassing π), to an extent that was significantly greater than for all other delta bins. Circle plots (top) are provided for visualization purposes and show the neural phase yielding the peak hit rate separately for the theta and alpha frequency bands. p values correspond to spherical Rayleigh tests for theta and alpha phases considered together (FDR corrected).

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    Figure 5.

    Gap-detection performance was determined by distinct delta–governed neural microstates. a, When hit rates were determined by delta phase alone (Microstate A), by a combination of delta and high-alpha phase (Microstate B), and by a combination of delta, theta, and low-alpha phase, gap-detection hit rates were relatively high when the local near trough-to-rising phase (highlighted in blue, pink, and green, respectively) of the complex neural activity coincided with gap onset (insets). Single-participant (thin, colored lines) and mean (thick, black lines) time course data corresponded well to the schematic microstates. Insets compare time courses preceding detected (hits, blue, pink, green) and undetected (misses, gray dashed lines) gaps. The time courses differed significantly (marked by gray bars below time courses) in time ranges corresponding to our analysis based on circular–linear correlations (Fig. 2, marked by colored shaded bars), and polarity was more negative preceding hits than misses. Topographies show the strength of consistency across participants in terms of optimal neural phase for gap-detection performance. b, Time courses of microstate prevalence (shown here for three representative participants) revealed slow fluctuations in the prevalence of individual microstates as well as gap-detection performance that had an average rate of 0.003 Hz across participants (bottom).

  • Figure 6.
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    Figure 6.

    a, Cochlea-scaled entropy was not significantly correlated with gap-detection hit rates (y-axis shows z-transformed correlation coefficients as a function of pre-gap time); gray dots show single-participant data, and black dots show mean data. b, Neither horizontal (left) nor vertical (right) EOG activity was correlated with delta phase. c, Horizontal EOG activity (left) was not correlated with hit rate, but vertical EOG (middle) activity was negatively correlated with gap-detection hit rates in a brief time window that did not overlap with the neural phase effects (highlighted gray). The right panel shows hit rates as a function of vertical EOG eye-movement magnitude (percentile, mean ± SEM).

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The Journal of Neuroscience: 36 (3)
Journal of Neuroscience
Vol. 36, Issue 3
20 Jan 2016
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Neural Microstates Govern Perception of Auditory Input without Rhythmic Structure
Molly J. Henry, Björn Herrmann, Jonas Obleser
Journal of Neuroscience 20 January 2016, 36 (3) 860-871; DOI: 10.1523/JNEUROSCI.2191-15.2016

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Neural Microstates Govern Perception of Auditory Input without Rhythmic Structure
Molly J. Henry, Björn Herrmann, Jonas Obleser
Journal of Neuroscience 20 January 2016, 36 (3) 860-871; DOI: 10.1523/JNEUROSCI.2191-15.2016
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Keywords

  • auditory perception
  • entrainment
  • neural microstates
  • neural oscillations
  • psychophysics

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