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Research ArticleResearch Article: Confirmation, Sensory and Motor Systems

Robustness to Noise in the Auditory System: A Distributed and Predictable Property

S. Souffi, C. Lorenzi, C. Huetz and J.-M. Edeline
eNeuro 25 February 2021, 8 (2) ENEURO.0043-21.2021; https://doi.org/10.1523/ENEURO.0043-21.2021
S. Souffi
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Department Integrative and Computational Neuroscience, Unité Mixte de Recherche (UMR 9197) Centre National de la Recherche Scientifique Orsay 91405, France
2Université Paris-Saclay, Orsay Cedex 91405, France
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C. Lorenzi
3Laboratoire des Systèmes Perceptifs, Unité Mixte de Recherche (UMR 8248) Centre National de la Recherche Scientifique, Département d’Etudes Cognitives, Ecole Normale Supérieure, Université Paris Sciences et Lettres, Paris 75005, France
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C. Huetz
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Department Integrative and Computational Neuroscience, Unité Mixte de Recherche (UMR 9197) Centre National de la Recherche Scientifique Orsay 91405, France
2Université Paris-Saclay, Orsay Cedex 91405, France
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J.-M. Edeline
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Department Integrative and Computational Neuroscience, Unité Mixte de Recherche (UMR 9197) Centre National de la Recherche Scientifique Orsay 91405, France
2Université Paris-Saclay, Orsay Cedex 91405, France
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Figures

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  • Figure 1.
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    Figure 1.

    Original and noisy vocalizations. A, Waveforms (top) and spectrograms (bottom) of the four original whistles used in this study. B, C, Spectrograms of the four whistles in stationary (B) and chorus (C) noise at three SNRs (+10, 0, and −10 dB, from top to bottom) and the noise only. The frequency range for all spectrograms is 0–30 kHz, and all spectrograms share the same color scale (covering a range of 50 dB).

  • Figure 2.
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    Figure 2.

    The decrease in EI values is more pronounced in chorus noise than in stationary noise in each auditory structure. A, Raster plots of responses of the four original vocalizations, noisy vocalizations (in both noises), and noise alone recorded in CN, CNIC, MGv, A1, and VRB. The gray part of rasters corresponds to the evoked activity. For each structure, all the rasters correspond to the same recording. B, Rasters showing examples of neuronal responses in stationary noise with values of EI > 0 corresponding to a signal-like response (left, IC recording) and EI < 0 corresponding to a masker-like response (right, A1 recording). Top panels show the responses to the original vocalizations, the middle panels the responses to vocalizations at the 0-dB SNR in stationary noise and the bottom panels the responses to stationary noise alone. C, Box plots showing the EI values for the three SNRs obtained in CN (in black), CNIC (in green), MGv (in orange), A1 (in blue), and VRB (in purple) alternatively in stationary noise (SN) and chorus noise (CN). In each box plot, the red dot represents the mean value. The black lines represent significant differences between the mean values (one-way ANOVAs, p < 0.001; with post hoc paired t tests, pa+10 dB,CN = 4.03e-18, pb+10 dB, CNIC = 1.45e-07, pc0dB, CNIC = 2.47e-45, pd0dB, MGv = 2.11e-30, pe0dB, A1 = 5.41e-25, pf0dB,VRB = 6.36e-10, pg-10 dB, CN = 5.74e-12, ph-10 dB, CNIC = 1.83e-59, pi-10 dB, MGv = 1.16e-36, pj-10 dB, A1 = 2.84e-24, pk+10 dB, VRB = 4.62e-11).

  • Figure 3.
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    Figure 3.

    The choice of five clusters is optimal to reveal the different behaviors in both noises. A, Mean square error of EI profile clustering as a function of the number of clusters using the K-means algorithm for the stationary and chorus noise. B, C, Population average EI profile (±SEM) of each cluster when considering six clusters to separate the data in the stationary noise (B) and in the chorus noise (C). Note that in both noises, two clusters have similar mean EI profile, i.e., the same EI evolution across the three SNRs (the two gray clusters in B and the two blue clusters in C) leading us to consider only five clusters in the following results (Fig. 4).

  • Figure 4.
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    Figure 4.

    Robustness to noise is a distributed property in the auditory system. A, Each row corresponds to the EI profile of a given neuronal recording obtained in the five auditory structures in stationary noise with a color code from blue to red when progressing from low to high EI values. On the right, five stacked colors delineate the identity for the five categories of responses. The signal-like category is in green, the signal-dominated category in pink, the balanced category in turquoise, the insensitive category in gray and the masker-like category in yellow. The names of the categories used in the study by Ni et al. (2017) are provided for comparison. B–E. 3D representation of the five categories in stationary noise (B), mean EI values (±SEM) of the five categories (C), relative proportions of each category in stationary noise (D), and proportion of each category in the five auditory structures from CN to VRB (E). F–J, Same representations as in A–E for the responses collected in the chorus noise. See Table 1, selection type (b), for referring to the number of selected recordings in each structure.

  • Figure 5.
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    Figure 5.

    The noise-type sensitivity is found at each stage of the auditory system. A1, Group-switching matrix representing the percentage of recordings in a given category in chorus noise depending on the category originally assigned in the stationary noise. The abscissas indicate the category identity in the stationary noise, and the ordinates represent the category identity in the chorus noise. For example, signal-like responses in stationary noise are also 50% signal-like in chorus noise but 10% are reclassified as signal-dominated, 35% balanced, 1.5% insensitive, and 3.5% masker-like. Note that, in stationary noise, the number of recordings in each category were 139, 346, 83, 540, and 159 in signal-like, signal-dominated, balanced, insensitive, and masker-like category, respectively. A2, Mean percentages of recordings changing category from the stationary noise to the chorus noise, first in each category and second in each structure [VRB, (in purple), A1 (in blue), MGv (in orange), CNIC (in green), and CN (in black)]. B1, Group-switching matrix representing the percentages of recordings changing category from the stationary noise to the chorus noise based only on recordings considered as reliable with the bootstrap procedure in the two types of noise (with a confidence interval ⩾95%). B2, Mean percentages of recordings changing category from the stationary noise to the chorus noise, first in each category and second in each structure [VRB, (in purple), A1 (in blue), MGv (in orange), CNIC (in green), and CN (in black)].

  • Figure 6.
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    Figure 6.

    Descriptors of the categories in stationary noise used by the classifiers. A–C, Three TFRP parameters were chosen as descriptors: the BF firing rate, the bandwidth and the response duration. D, E, Two signal descriptors were selected corresponding to the firing rate and the CorrCoef values obtained in original conditions. F, G, Two main masker descriptors were presented corresponding to the firing rate and the CorrCoef values obtained in stationary noise alone. H, I, The three other masker descriptors are: (H) the ratio between the masker firing rate taken at the time the signal should have occurred and the initial masker firing rate during the first 200 ms of the masker and the number of action potentials emitted during the first (initial; I) and last (final, I) 50 ms of the masker alone over a 564-ms period. J, K, Two descriptors of the signal-to-masker ratio are presented and taken into account the firing rate of responses to the signal and to the masker; the two differ only on which part of the response to the masker is taken into account (see Materials and Methods). For each violin plot, the red dot represents the median value and the black lines represent significant differences between the median values (Kruskal–Wallis test, p < 0.05).

  • Figure 7.
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    Figure 7.

    Descriptors of the categories in chorus noise used by the classifiers. A–C, Three TFRP parameters were chosen as descriptors: the BF firing rate, the bandwidth and the response duration. D, E, Two signal descriptors were selected corresponding to the firing rate and the CorrCoef values obtained in original conditions. F, G, Two main masker descriptors were presented corresponding to the firing rate and the CorrCoef values obtained in chorus noise alone. H, I, The three other masker descriptors are: (H) the ratio between the masker firing rate taken at the time the signal should have occurred and the initial masker firing rate during the first 200 ms of the masker and the number of action potentials emitted during the first (initial; I) and last (final; I) 50 ms of the masker alone over a 564-ms period. J, K, Two descriptors of the signal-to-masker ratio are presented and taken into account the firing rate of responses to the signal and to the masker; the two differ only on which part of the response to the masker is taken into account (see Materials and Methods). For each violin plot, the red dot represents the median value and the black lines represent significant differences between the median values (Kruskal–Wallis test, p < 0.05).

  • Figure 8.
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    Figure 8.

    The neuronal behaviors in stationary and chorus noise are predictable based on response parameters obtained in quiet. A, All tested combinations (1–15) based on four types of descriptors (TFRP, signal, masker, and signal/masker) of the categories in stationary noise and their respective percentages of accuracy of the classifier. The gray part means that the descriptor is included in the classifier and the white part means that the descriptor is excluded from the classifier. B, C, Example of the confusion matrix obtained with all descriptors (combination 1) in stationary (B) and chorus (C) noise. Each row corresponds to a true category and each column corresponds to a predicted category. The numbers in the confusion matrix correspond to the percentage of recordings of a given true category which have been predicted to belong to a given predicted category.

  • Figure 9.
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    Figure 9.

    Generalization of the classification. In this figure, the classifiers were trained with the reliable neurons and tested on the rest of the population. All tested combinations (1–15) based on four types of descriptors (TFRP, signal, masker, and signal/masker) of the categories in stationary and chorus noise and their respective percentages of accuracy of the classifier. The gray part means that the descriptor is included in the classifier and the white part means that the descriptor is excluded from the classifier.

Tables

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    Table 1

    Summary of the number of animals and number of selected recordings in each structure.

    CNLemniscal
    pathway
    Non-lemniscal
    pathway
    Total
    CNICMGvA1VRB
    Number of animals10111011547
    Number of recordings tested6724784485441922334
    Six EI values (for the six SNRs)6174333434881842065
    One of the six EI values significantly higher than the EISurrogate4283742303491371518
    Selection type
     (a) Significant response to at least one vocalization and/or significant TFRP4013502102791091349
     (b) Significant response to at least one vocalization and significant TFRP389339198261801267
    • CN: cochlear nucleus, CNIC: central nucleus of inferior colliculus, MGv: ventral part of the MGB, A1: primary auditory cortex, VRB: ventrorostral belt.

    • A recording corresponds to a channel of a 16-channel electrode.

    • View popup
    Table 2

    Number of recordings reliably categorized both in stationary and in chorus noise using the bootstrap procedure and number of recordings sensitive to the type of noise within this population

    CNLemniscal
    pathway
    Non-lemniscal
    pathway
    Total
    CNICMGvA1VRB
    Number of recordings reliably categorized in the two noises13980505221342
    Number of recordings reliably categorized and noise-type sensitive3035361210123
    Number of recordings reliably categorized and no noise-type sensitive10945144011219

Extended Data

  • Figures
  • Tables
  • Extended Data Figure 4-1

    Similar results as in Figure 4 are obtained taking into account the neurons without significant TRFP. A–C, Mean EI values (±SEM) of the five categories across the three SNRs (+10, 0, and –10 dB; A), relative proportions of each category in stationary noise (B) and proportion of each category in the five auditory structures from CN to VRB for the recordings with or without significant TFRP (relative to pure tone responses; C). D, Proportion of each category in the five auditory structures from CN to VRB for the recordings without significant TFRP. E–H, Same representations as in A–D for the chorus noise. See Table 1, selection type (a), for referring to the number of selected recordings in each structure. Download Figure 4-1, TIF file.

  • Extended Data Figure 4-2

    Attempt to separate the ventral and dorsal parts of the CN based on the depth of the recordings. A, B, Box plots showing the EI values for the three SNRs obtained in the ventral (VCN, in black) and dorsal (DCN, in grey) parts of the CN in stationary noise (A) and chorus noise (B). In each box plot, the red dot represents the mean value. There was no significant difference between the EI values obtained in VCN and DCN for the three SNRs and in both noises (one-way ANOVAs, p > 0.05; with post hoc paired t tests, p > 0.05). C, Proportion of each category in the ventral part of the CN (VCN, n = 87 recordings) and its dorsal part (DCN, n = 302 recordings) obtained in stationary (SN) and chorus (CN) noise. Download Figure 4-2, TIF file.

  • Extended Data Figure 4-3

    Lemniscal and non-lemniscal parts of the IC. Proportion of each category in the lemniscal part of IC (CNIC, n = 339 recordings) and its non-lemniscal parts (dorsal and external cortices of the IC, DCIC-ECIC, n = 73 recordings) obtained in stationary and chorus noise. See Table 1, selection type (b), for referring to the number of selected recordings. Download Figure 4-3, TIF file.

  • Extended Data Figure 5-1

    Confusion matrices obtained for all and reliable recordings. A, Confusion matrix relative to Figure 5A1 representing the number of recordings in a given category in chorus noise depending on the category originally assigned in the stationary noise. B, Same as in A with only recordings considered as reliable with the bootstrap procedure in the two types of noise (with a confidence interval ⩾95%). This figure is relative to the Figure 5B1. Note that the MI (bits) values were low in A, B corroborating the fact that a large proportion of recordings assigned to a given category in stationary noise change category in chorus noise. Download Figure 5-1, TIF file.

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Robustness to Noise in the Auditory System: A Distributed and Predictable Property
S. Souffi, C. Lorenzi, C. Huetz, J.-M. Edeline
eNeuro 25 February 2021, 8 (2) ENEURO.0043-21.2021; DOI: 10.1523/ENEURO.0043-21.2021

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Robustness to Noise in the Auditory System: A Distributed and Predictable Property
S. Souffi, C. Lorenzi, C. Huetz, J.-M. Edeline
eNeuro 25 February 2021, 8 (2) ENEURO.0043-21.2021; DOI: 10.1523/ENEURO.0043-21.2021
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Keywords

  • auditory system
  • natural vocalizations
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  • neuronal classification
  • noise-type sensitivity

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