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Research ArticleNew Research, Sensory and Motor Systems

Distinct Correlation Structure Supporting a Rate-Code for Sound Localization in the Owl’s Auditory Forebrain

Michael V. Beckert, Rodrigo Pavão and José L. Peña
eNeuro 26 June 2017, 4 (3) ENEURO.0144-17.2017; https://doi.org/10.1523/ENEURO.0144-17.2017
Michael V. Beckert
Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461
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Rodrigo Pavão
Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461
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José L. Peña
Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461
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  • Figure 1.
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    Figure 1.

    Schematic of tectal (blue) and forebrain (red) auditory pathways of the owl’s brain. The auditory midbrain consists of subdivisions of the inferior colliculus: the central core (ICc), lateral shell (ICls), and external nucleus (ICx). The map of auditory space first emerges in ICx. ICx projects to the OT, analog to the superior colliculus. The forebrain pathway originates in projections from the inferior colliculus to the thalamus. The auditory forebrain structure Field L, analog to primary auditory cortex, displays a clustered nontopographic tuning to binaural cues. Field L projects directly to the AAr, analog to the auditory portion of the frontal eye fields. AAr sends projections back onto OT. For clarity, some connections are omitted.

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    Figure 2.

    Azimuth tuning of nearby neurons in OT. A, Spatial receptive field (SpRF) (top) and azimuth tuning curve (bottom) obtained by averaging the SpRF across elevation. B, Peristimulus time histogram (PSTH; top) and raster (bottom) for the spiking activity of the neuron in A responding to sound at the preferred direction (90° azimuth and 0° elevation). C, Example azimuth tuning curves of neurons recorded from the same site. Responses are normalized to facilitate visual comparison. Tuning curves represent mean ± SEM, 20–40 repetitions.

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    Figure 3.

    Azimuth tuning in Field L. A, Example SpRFs (top) and azimuth tuning curves (bottom) of Field L neurons from different recording sites. B, Peristimulus time histogram (PSTH; top) and rasters (bottom) for the spiking activity of the neurons in A for sounds from the speakers eliciting the maximal response. C, Example azimuth tuning curves of neurons recorded from the same site (different neurons from A, B). Firing rates are normalized to facilitate comparison. Tuning curves represent mean ± SEM, 20–40 repetitions. D, Rsig for azimuth tuning of nearby cells (left) and cells from different recording sites (right). Box plots show median (red line), interquartile range (blue), and 5% and 95% quantiles (whiskers). Black dots indicate the sorted distribution of data points. Asterisks indicate statistical significance (****p < 0.0001; two-tailed Mann–Whitney U test).

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    Figure 4.

    Spatial tuning in AAr. A, Example SpRF (top) and azimuth tuning curve (bottom). B, Peristimulus time histogram (PSTH; top) and rasters (bottom) for the spiking activity of the neuron in A, stimulated by sound from the speaker that elicited the maximal response (20° azimuth and −20° elevation). C, Example azimuth tuning curves of neurons recorded from the same site. Curves show normalized firing (mean ± SEM, 20–40 repetitions). D, Signal correlation for azimuth tuning of nearby cells (left) and cells from different recording sites (right). E, Overlaid azimuth tuning curves of all neurons in the AAr dataset. F, Signal correlation within ipsilateral, frontal, and contralateral azimuth subregions of distant cells. G, Steepness (slope) of azimuth tuning curves within ipsilateral, frontal, and contralateral space. Box plots in D, F, G show median (red line), interquartile range (blue), and 5% and 95% quantiles (whiskers). Black dots indicate the sorted distribution of data points. ****p < 0.0001. D, Two-tailed Mann–Whitney U test; F, G, Kruskal-Wallis H test with Dunn’s multiple comparisons correction.

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    Figure 5.

    Comparison of signal correlation across brain regions. A, Signal correlation in nearby cells for azimuth tuning. B, C, Signal correlation across recording sites, for azimuth (B) and ITD (C) tuning. The significantly stronger signal correlation across distant cells in AAr corroborates a more homogeneous tuning than in Field L. Box plots show median (red line), interquartile range (blue), and 5% and 95% quantiles (whiskers). Black dots indicate the sorted distribution of raw values. ***p < 0.001, ****p < 0.0001. A, Kruskal-Wallis H test with Dunn’s multiple comparisons correction; B, C, two-tailed Mann–Whitney U test.

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    Figure 6.

    Comparison of RNCs. A, RNCs in OT, Field L, and AAr. B, Average firing rates of OT, Field L, and AAr cells during sound presentation (left) and spontaneous firing (right). C, D, Average variance (C) and covariance (D) in OT, Field L, and AAr neurons. Box plots represent median (red line), interquartile range (blue), and 5% and 95% quantiles (whiskers). Black dots indicate the sorted distribution of raw values. *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001; Kruskal-Wallis H test with Dunn’s multiple comparisons correction.

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    Figure 7.

    Spike-time synchrony in OT, Field L, and AAr. A, Example CCGs for pairs of evoked (left) and spontaneous (right) responses in OT (top), Field L (middle), and AAr (bottom). The corrected CCGs for individual pairs of neurons (solid black) are overlaid to the smoothed CCG (dashed green) and shifted CCG (dashed orange). The plots for left and right are from the same pair. B, C, Statistical comparison of synchrony across brain regions for evoked (B) and spontaneous (C) spikes. Box plots represent median (red line), interquartile range (blue), and 5% and 95% quantiles (whiskers). Black dots indicate the sorted data; **p < 0.01, ****p < 0.0001; Kruskal-Wallis H test with Dunn’s multiple comparisons correction.

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    Figure 8.

    Decoding of ITD and azimuth from firing rate. A, Decoding accuracy in pairs of simultaneously recorded units in OT, Field L, and AAr. Box plots represent median (red line), interquartile range (blue), and 5% and 95% quantiles (whiskers). Asterisks indicate better than chance level decoding of azimuth (dashed line: 14.92°). Dots are the sorted data points. B–D, left, Decoder performance (colored points) plotted against signal (Rsig) and RNC for each pair of neurons in OT (B), Field L (C), and AAr (D). Point color indicates level of accuracy (color bar on the right). Right, Linear fit of accuracy data as a function of signal and RNC. White dashed ellipsoids depict 95% range of signal and RNCs used for the linear fit, which avoided outliers. Fit functions and R 2 values are shown above each plot. Color bar matches all plots (****p < 0.0001; Wilcoxon signed-rank test).

  • Figure 9.
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    Figure 9.

    Summary of findings. Top, Large-scale spatial tuning organization of each region (above) and corresponding schematic tuning curves at recording locations (below) denoted by crosses (X1 and X2 represent nearby sites) and triangles representing a distant site. OT displays a topographic organization of spatial tuning, while Field L is organized in clusters. AAr displays uniform tuning. Middle, Signal correlation for distant (above) and nearby (below) neurons. Tuning curves of distant sites is different in OT (extrapolated from previous descriptions) and Field L but similar in AAr (insets). On the other hand, tuning curves of nearby neurons are similar in all three structures. Scatter plots represent firing rates (FR) of pairs of cells across azimuth plotted against one another, used to calculate signal correlation. Tuning curves are shown in the insets. Bottom, Schematic scatter plots representing the correlated FR variability of nearby cells in OT, intermediate level of FR variability in Field L, and uncorrelated FR variability in AAr.

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    Table 1.

    Summary of statistics

    Source figureTestSample size (n)Test statisticspPower α = 0.05
    3DMann-Whitney UWithin, 300; across, 4068U = 301,457<0.00011
    4DMann-Whitney UWithin, 252; across, 5874U = 559,821<0.00010.99
    4FKruskal-Wallis HFull, 5875; ipsilateral, 5791; frontal, 5874; contralateral, 5874H = 23,413<0.0001 for all1
    4GKruskal-Wallis HIpsilateral, 700; frontal, 700; contralateral, 700H = 533.1<0.0001 for all1
    5AKruskal-Wallis HOT, 193; Field L, 300; AAr, 252H = 19.3OT vs Field L = 0.0006 Field L vs AAr = 0.00071
    5BMann-Whitney UField L, 4068; AAr, 5974U = 5,671,377<0.00011
    5CMann-Whitney UField L, 469; AAr, 493U = 361,864<0.00010.99
    6AKruskal-Wallis HOT, 168; Field L, 225; AAr, 48H = 8.93OT vs AAr = 0.00880.985
    6BKruskal-Wallis HOT, 332; Field L, 259; AAr, 302H = 95.6OT vs Field L < 0.0001 OT vs AAr = 0.0003 Field L vs AAr < 0.00011
    6BKruskal-Wallis HOT, 359; Field L, 268; AAr, 323H = 90.6OT vs AAr < 0.0001 Field L vs AAr < 0.00011
    6CKruskal-Wallis HOT, 102; Field L, 121; AAr, 142H = 63.7OT vs FL < 0.0001; OT vs AAr = 0.0093 FL vs AAr < 0.00011
    6DKruskal-Wallis HOT, 232; Field L, 294; AAr, 235H = 28.9OT vs FL < 0.0001; OT vs AAr = 0.0049 FL vs AAr = 0.0341
    7BKruskal-Wallis HOT, 116; Field L, 102; AAr, 219H = 172.4OT vs AAr < 0.0001 Field L vs AAr < 0.00011
    7CKruskal-Wallis HOT, 136; Field L, 83; AAr, 207H = 184OT vs FL = 0.0067 OT vs AAr < 0.0001; FL vs AAr < 0.00011
    8AWilcoxon TOT, 168T = 14,196<0.00011
    8AWilcoxon TField L, 225T = 25,425<0.00011
    8AWilcoxon TAAr, 48T = 1,176<0.00011
    • Test statistics; U for Mann-Whitney, H for Kruskal-Wallis, and T for Wilcoxon.

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Distinct Correlation Structure Supporting a Rate-Code for Sound Localization in the Owl’s Auditory Forebrain
Michael V. Beckert, Rodrigo Pavão, José L. Peña
eNeuro 26 June 2017, 4 (3) ENEURO.0144-17.2017; DOI: 10.1523/ENEURO.0144-17.2017

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Distinct Correlation Structure Supporting a Rate-Code for Sound Localization in the Owl’s Auditory Forebrain
Michael V. Beckert, Rodrigo Pavão, José L. Peña
eNeuro 26 June 2017, 4 (3) ENEURO.0144-17.2017; DOI: 10.1523/ENEURO.0144-17.2017
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