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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Contributions of Distinct Auditory Cortical Inhibitory Neuron Types to the Detection of Sounds in Background Noise

Anna A. Lakunina, Nadav Menashe and Santiago Jaramillo
eNeuro 15 February 2022, 9 (2) ENEURO.0264-21.2021; DOI: https://doi.org/10.1523/ENEURO.0264-21.2021
Anna A. Lakunina
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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Nadav Menashe
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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Santiago Jaramillo
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene, Oregon 97403
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  • Figure 1.
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    Figure 1.

    Performance in a signal detection task. A, Schematic of the signal detection task. Mice had to correctly report the presence or absence of a pure tone signal to obtain a reward. B, Example frequency spectra of sounds used during the signal detection task. C, Example psychometric curve showing the performance of one mouse during one behavior session. Performance is averaged over all masker bandwidths presented. Error bars show 95% confidence intervals. D, Median psychometric curve (black line) for mice trained in the signal detection task (N = 48 mice). Psychometric curves for individual mice are shown in gray. Trials are pooled across multiple sessions. Performance is averaged over all masker bandwidths presented.

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    Figure 2.

    Location of optical fibers. Coronal brain slice showing the location of optical fibers implanted above the auditory cortex, such that light was concentrated on the AUDp. The primary field is surrounded by a dorsal and a ventral field (AUDd and AUDv, respectively). Laser powers were chosen such that areas outside the auditory cortex were unlikely to be affected. SS, Somatosensory cortex; TEa, temporal association area; HC, hippocampus. Scale bar, 1 mm.

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    Figure 3.

    Inactivation of the auditory cortex impaired the detection of signals masked by noise. A, Top, Optogenetic stimulation in freely moving PV::ChR2 mice. Laser activation of PV+ cells in the auditory cortex silences auditory cortical activity. Bottom, For a random 25% of trials in each session, the laser turned on at the same time as the sound and lasted for 100 ms after the sound turned off. B, Example psychometric curve from one PV::ChR2 mouse trained to report the presence of the tone by going to the right (trials pooled across multiple sessions). The activation of auditory cortical PV+ cells reduced the probability of the mouse reporting the presence of the tone for all SNRs. Error bars show 95% confidence intervals. C, Like B, but for a PV::ChR2 mouse trained to go to the left to report the presence of the tone. As before, the activation of auditory cortical PV+ cells reduced the probability of the tone being reported, despite the opposite action being required to report tones. D, Silencing the auditory cortex during the signal detection task significantly reduced sensitivity to the pure tone signal (p = 0.0117, Wilcoxon signed-rank test; N = 8 mice). Each pair of points corresponds to one mouse. E, Silencing the auditory cortex during the signal detection task significantly reduced the hit rate (p = 0.0117, Wilcoxon signed-rank test). F, Silencing the auditory cortex during the signal detection task significantly reduced the false alarm rate (p = 0.0251, Wilcoxon signed-rank test). G, The effect of silencing the auditory cortex (No AC) on d′ was not correlated with the effect of visual distraction (Control) on d′ (p = 0.593, r = 0.224, linear correlation coefficient). Each point corresponds to one mouse. H, The effect of silencing the auditory cortex on hit rate was not correlated with the effect of visual distraction on hit rate (p = 0.157, r = 0.710, linear correlation coefficient). I, The effect of silencing the auditory cortex on false alarm rate was not correlated with the effect of visual distraction on false alarm rate (p = 0.589, r = 0.227, linear correlation coefficient).

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    Figure 4.

    Inactivation of the auditory cortex yielded consistent impairments across sessions. Signal detection performance (d′) during each behavioral session (dots) compared with the pooled performance across all trials (horizontal lines) for each PV::ChR2 mouse (M1–M8).

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    Figure 5.

    Inactivation of the auditory cortex did not affect the timing of behavior. A, Silencing the auditory cortex during the signal detection task did not affect the time spent sampling the sound in the center port (p = 0.0925, Wilcoxon signed-rank test; N = 8 mice). Each pair of points corresponds to one mouse. B, Silencing the auditory cortex during the signal detection task did not affect the time spent moving toward the reward port (p = 0.779, Wilcoxon signed-rank test). Each point corresponds to one mouse. C, The effect of silencing the auditory cortex (No AC) on time spent sampling the sound in the center port was not correlated with the effect of visual distraction (control) on sampling time (p = 0.675, r = 0.177; linear correlation coefficient). D, The effect of silencing the auditory cortex on time spent moving toward the reward port was not correlated with the effect of visual distraction on time spent moving toward the reward port (p = 0.686, r = –0.171; linear correlation coefficient).

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    Figure 6.

    Contributions of distinct inhibitory neuron types to auditory signal detection. A, Inactivation of PV+ cells during the signal detection task. Laser was presented for a random 25% of trials each session. B, Example psychometric curve from one PV::ArchT mouse (trials pooled across multiple sessions). Inactivation of auditory cortical PV+ cells decreased the probability of the mouse reporting hearing the signal when it was present, though false alarm rate was unaffected. Error bars show 95% confidence intervals. C, Inactivating auditory cortical PV+ cells during the signal detection task significantly reduced sensitivity to the signal (p = 0.0046, Wilcoxon signed-rank test; N = 13 mice). D, Inactivating auditory cortical PV+ cells during the signal detection task significantly reduced the hit rate (p = 0.033, Wilcoxon signed-rank test). E, Inactivating auditory cortical PV+ cells during the signal detection task did not significantly affect the false alarm rate (p = 0.861, Wilcoxon signed-rank test). F, The effect of inactivating auditory cortical PV+ cells (No PV) on d′ was not correlated with the effect of visual distraction (control) on d′ (p = 0.609, r = 0.157; linear correlation coefficient). G, The effect of inactivating auditory cortical PV+ cells on hit rate was not correlated with the effect of visual distraction on hit rate (p = 0.657, r = –0.136; linear correlation coefficient). H, The effect of inactivating auditory cortical PV+ cells on false alarm rate was not correlated with the effect of visual distraction on false alarm rate (p = 0.981, r = –0.0073; linear correlation coefficient). I, Inactivation of SOM+ cells during the signal detection task. Laser was presented for a random 25% of trials each session. J, Like B, but for one SOM::ArchT mouse. Inactivation of auditory cortical SOM+ cells reduced the probability of the mouse reporting hearing the signal when it was present, though false alarm rate was unaffected. K, Inactivating auditory cortical SOM+ cells during the signal detection task significantly reduced sensitivity to the signal (p = 0.0051, Wilcoxon signed-rank test; N = 10 mice). L, Inactivating auditory cortical SOM+ cells during the signal detection task significantly reduced the hit rate (p = 0.0051, Wilcoxon signed-rank test). M, Inactivating auditory cortical SOM+ cells during the signal detection task did not significantly affect the false alarm rate (p = 0.878, Wilcoxon signed-rank test). N, The effect of inactivating auditory cortical SOM+ cells (No SOM) on d′ was not correlated with the effect of visual distraction (control) on d′ (p = 0.546, r = 0.218; linear correlation coefficient). O, The effect of inactivating auditory cortical SOM+ cells on hit rate was correlated with the effect of visual distraction on hit rate (p = 0.0494, r = 0.633; linear correlation coefficient). P, The effect of inactivating auditory cortical SOM+ cells on false alarm rate was not correlated with the effect of visual distraction on false alarm rate (p = 0.0725, r = 0.590; linear correlation coefficient).

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    Figure 7.

    Effects of disrupting auditory cortical inhibition on each behavioral session. Signal detection performance (d′) during each behavioral session (dots) compared with the pooled performance across all trials (horizontal lines) for each PV::ArchT mouse (PV1–PV13) and each SOM::ArchT mouse (SOM1–SOM10). B, Baseline (laser off); M, manipulation (laser on).

  • Figure 8.
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    Figure 8.

    Inactivation of distinct inhibitory neuron types did not affect the timing of behavior. A, Inactivating auditory cortical PV+ cells during the signal detection task did not affect the time spent sampling the sound in the center port (p = 0.0652, Wilcoxon signed-rank test). B, The effect of inactivating auditory cortical PV+ cells (No PV) on the time spent sampling the sound in the center port was correlated with the effect of visual distraction (control) on sampling time (p = 0.0017, r = 0.780; linear correlation coefficient). C, Inactivating auditory cortical PV+ cells during the signal detection task led to a small (1.8%) but statistically significant increase in the time spent obtaining a reward (p = 0.0029, Wilcoxon signed-rank test). D, The effect of inactivating auditory cortical PV+ cells on the time spent obtaining a reward was not correlated with the effect of visual distraction on the time spent obtaining a reward (p = 0.901, r = 0.0383; linear correlation coefficient). E, Inactivating auditory cortical SOM+ cells during the signal detection task significantly increased the time spent sampling the sound in the center port, leading to a median increase in sampling time of 3.7% (p = 0.005, Wilcoxon signed-rank test). F, The effect of inactivating auditory cortical SOM+ cells (No SOM) on sampling time was not correlated with the effect of visual distraction (control) on sampling time (p = 0.901, r = 0.0453; linear correlation coefficient). G, Inactivating auditory cortical SOM+ cells during the signal detection task did not affect the time spent obtaining a reward (p = 0.203, Wilcoxon signed-rank test). H, The effect of inactivating auditory cortical SOM+ cells on the time spent obtaining a reward was not correlated with the effect of visual distraction on the time spent obtaining a reward (p = 0.470, r = 0.259; linear correlation coefficient).

Tables

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    Table 1

    Summary of statistical analyses

    FigureMeasurementComparisonStatistical testTest results
    3Dd′Without laser presentation vs with laser presentation (N = 8 PV::ChR2 mice)Wilcoxon signed-rank testp = 0.0117, T = 0
    3EHit rate (%)Without laser presentation vs with laser presentation (N = 8 PV::ChR2 mice)Wilcoxon signed-rank testp = 0.0117, T = 0
    3FFalse alarm rate (%)Without laser presentation vs with laser presentation (N = 8 PV::ChR2 mice)Wilcoxon signed-rank testp = 0.0251, T = 2
    3GLaser-induced change in d′Laser directed at AC vs laser directed away from AC (N = 8 PV::ChR2 mice)Correlation coefficientp = 0.593 r = 0.224
    3HLaser-induced change in hit rate (%)Laser directed at AC vs laser directed away from AC (N = 8 PV::ChR2 mice)Correlation coefficientp = 0.710, r = 0.157
    3ILaser-induced change in false alarm rate (%)Laser directed at AC vs laser directed away from AC (N = 8 PV::ChR2 mice)Correlation coefficientp = 0.589, r = 0.227
    5ASampling time (ms)Without laser presentation vs with laser presentation (N = 8 PV::ChR2 mice)Wilcoxon signed-rank testp = 0.0925, T = 6
    5BTime to reward (ms)Without laser presentation vs with laser presentation (N = 8 PV::ChR2 mice)Wilcoxon signed-rank testp = 0.779, T = 16
    5CLaser-induced change in sampling time (ms)Laser directed at AC vs laser directed away from AC (N = 8 PV::ChR2 mice)Correlation coefficientp = 0.675, r = 0.177
    5DLaser-induced change in time to reward (ms)Laser directed at AC vs laser directed away from AC (N = 8 PV::ChR2 mice)Correlation coefficientp = 0.686 r = –0.171
    6Cd′Without laser presentation vs with laser presentation (N = 13 PV::ArchT mice)Wilcoxon signed-rank testp = 0.0046, T = 5
    6DHit rate (%)Without laser presentation vs with laser presentation (N = 13 PV::ArchT mice)Wilcoxon signed-rank testp = 0.0330, T = 15
    6EFalse alarm rate (%)Without laser presentation vs with laser presentation (N = 13 PV::ArchT mice)Wilcoxon signed-rank testp = 0.861, T = 43
    6FLaser-induced change in d′Laser directed at AC vs laser directed away from AC (N = 13 PV::ArchT mice)Correlation coefficientp = 0.609, r = 0.157
    6GLaser-induced change in hit rate (%)Laser directed at AC vs laser directed away from AC (N = 13 PV::ArchT mice)Correlation coefficientp = 0.657 r = –0.136
    6HLaser-induced change in false alarm rate (%)Laser directed at AC vs laser directed away from AC (N = 13 PV::ArchT mice)Correlation coefficientp = 0.981 r = –0.0073
    6Kd′Without laser presentation vs with laser presentation (N = 10 SOM::ArchT mice)Wilcoxon signed-rank testp = 0.0051, T = 0
    6LHit rate (%)Without laser presentation vs with laser presentation (N = 10 SOM::ArchT mice)Wilcoxon signed-rank testp = 0.0051, T = 0
    6MFalse alarm rate (%)Without laser presentation vs with laser presentation (N = 10 SOM::ArchT mice)Wilcoxon signed-rank testp = 0.878, T = 26
    6NLaser-induced change in d′Laser directed at AC vs laser directed away from AC (N = 10 SOM::ArchT mice)Correlation coefficientp = 0.546, r = 0.218
    6OLaser-induced change in hit rate (%)Laser directed at AC vs laser directed away from AC (N = 10 SOM::ArchT mice)Correlation coefficientp = 0.0494, r = 0.633
    6PLaser-induced change in false alarm rate (%)Laser directed at AC vs laser directed away from AC (N = 10 SOM::ArchT mice)Correlation coefficientp = 0.0725, r = 0.590
    6Laser-induced change in d′Laser directed at AC in PV::ArchT mice (N = 13) vs SOM::ArchT mice (N = 10)Wilcoxon rank-sum testp = 0.321, T = 0.992
    8ASampling time (ms)Without laser presentation vs with laser presentation (N = 13 PV::ArchT mice)Wilcoxon signed-rank testp = 0.0652, T = 15.5
    8BLaser-induced change in sampling time (ms)Laser directed at AC vs laser directed away from AC (N = 13 PV::ArchT mice)Correlation coefficientp = 0.0017, r = 0.780
    8CTime to reward (ms)Without laser presentation vs with laser presentation (N = 13 PV::ArchT mice)Wilcoxon signed-rank testp = 0.0029, T = 1
    8DLaser-induced change in time to reward (ms)Laser directed at AC vs laser directed away from AC (N = 13 PV::ArchT mice)Correlation coefficientp = 0.901, r = 0.0383
    8ESampling time (ms)Without laser presentation vs with laser presentation (N = 10 SOM::ArchT mice)Wilcoxon signed-rank testp = 0.0050, T = 0
    8FLaser-induced change in sampling time (ms)Laser directed at AC vs laser directed away from AC (N = 10 SOM::ArchT mice)Correlation coefficientp = 0.901, r = 0.0453
    8GTime to reward (ms)Without laser presentation vs with laser presentation (N = 10 SOM::ArchT mice)Wilcoxon signed-rank testp = 0.203, T = 15
    8HLaser-induced change in time to reward (ms)Laser directed at AC vs laser directed away from AC (N = 10 SOM::ArchT mice)Correlation coefficientp = 0.470, r = 0.259
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Contributions of Distinct Auditory Cortical Inhibitory Neuron Types to the Detection of Sounds in Background Noise
Anna A. Lakunina, Nadav Menashe, Santiago Jaramillo
eNeuro 15 February 2022, 9 (2) ENEURO.0264-21.2021; DOI: 10.1523/ENEURO.0264-21.2021

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Contributions of Distinct Auditory Cortical Inhibitory Neuron Types to the Detection of Sounds in Background Noise
Anna A. Lakunina, Nadav Menashe, Santiago Jaramillo
eNeuro 15 February 2022, 9 (2) ENEURO.0264-21.2021; DOI: 10.1523/ENEURO.0264-21.2021
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Keywords

  • auditory cortex
  • cortical inhibition
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