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Efficient temporal processing of naturalistic sounds.

Lesica NA, Grothe B - PLoS ONE (2008)

Bottom Line: We find that the onset of ambient noise evokes a change in receptive field dynamics that corresponds to a change from bandpass to lowpass temporal filtering.We show that these changes occur within a few hundred milliseconds of the onset of the noise and are evident across a range of overall stimulus intensities.Using a simple model, we illustrate how these changes in temporal processing exploit differences in the statistical properties of vocalizations and ambient noises to increase the information in the neural response in a manner consistent with the principles of efficient coding.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology II, Ludwig-Maximilians-University Munich, Martinsried, Germany. lesica@zi.biologie.uni-muenchen.de

ABSTRACT
In this study, we investigate the ability of the mammalian auditory pathway to adapt its strategy for temporal processing under natural stimulus conditions. We derive temporal receptive fields from the responses of neurons in the inferior colliculus to vocalization stimuli with and without additional ambient noise. We find that the onset of ambient noise evokes a change in receptive field dynamics that corresponds to a change from bandpass to lowpass temporal filtering. We show that these changes occur within a few hundred milliseconds of the onset of the noise and are evident across a range of overall stimulus intensities. Using a simple model, we illustrate how these changes in temporal processing exploit differences in the statistical properties of vocalizations and ambient noises to increase the information in the neural response in a manner consistent with the principles of efficient coding.

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Context-dependent changes in temporal processing are robust to changes in the overall intensity of the stimulus.a–c) The RFs and MTFs for a typical cell estimated from responses to the V and VN stimuli at overall intensities of 25, 30, and 40 dB SPL above threshold. The preferred frequency of the cell was 10.1 KHz. The error bars represent 95% confidence bounds. The RFs were normalized to have the same peak value for plotting. Before computing the MTFs, RFs were normalized such that the variance of the result of the convolution of the RF with the vocalization signal was one. d) The LF areas of the V and VN MTFs at a range of intensities for the cell whose RFs and MTFs are shown in a–c. The error bars represent 95% confidence bounds. e) The percent change in LF area evoked by the addition of noise to the vocalization stimuli for a range of overall stimulus intensities for a sample of 8 cells. The error bars represent one standard deviation of the distribution of percent changes in LF area across the sample of cells.
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pone-0001655-g005: Context-dependent changes in temporal processing are robust to changes in the overall intensity of the stimulus.a–c) The RFs and MTFs for a typical cell estimated from responses to the V and VN stimuli at overall intensities of 25, 30, and 40 dB SPL above threshold. The preferred frequency of the cell was 10.1 KHz. The error bars represent 95% confidence bounds. The RFs were normalized to have the same peak value for plotting. Before computing the MTFs, RFs were normalized such that the variance of the result of the convolution of the RF with the vocalization signal was one. d) The LF areas of the V and VN MTFs at a range of intensities for the cell whose RFs and MTFs are shown in a–c. The error bars represent 95% confidence bounds. e) The percent change in LF area evoked by the addition of noise to the vocalization stimuli for a range of overall stimulus intensities for a sample of 8 cells. The error bars represent one standard deviation of the distribution of percent changes in LF area across the sample of cells.

Mentions: We also examined the effects of overall stimulus intensity on the observed changes in temporal processing. We estimated temporal RFs from responses to the V and VN stimuli across a range of overall stimulus intensities, as shown for a typical cell at intensities of 25, 30, and 40 dB SPL above threshold in figures 5a–c. The increase in the overall intensity of the stimulus evokes an increase in the LF areas of both the V and VN MTFs, as shown in figure 5d. Accordingly, the magnitude of the decrease in the LF area of the MTF evoked by the addition of noise to the vocalization increased as the overall intensity of the stimulus increased. However, for a sample of 8 cells, the percent decrease in the MTF LF area evoked by the addition of noise remained relatively constant across a range of intensities, as shown in figure 5e. We also found that the observed changes in temporal processing were robust to changes in the spectral properties of the carrier of the vocalization stimulus, as shown in Figure S1.


Efficient temporal processing of naturalistic sounds.

Lesica NA, Grothe B - PLoS ONE (2008)

Context-dependent changes in temporal processing are robust to changes in the overall intensity of the stimulus.a–c) The RFs and MTFs for a typical cell estimated from responses to the V and VN stimuli at overall intensities of 25, 30, and 40 dB SPL above threshold. The preferred frequency of the cell was 10.1 KHz. The error bars represent 95% confidence bounds. The RFs were normalized to have the same peak value for plotting. Before computing the MTFs, RFs were normalized such that the variance of the result of the convolution of the RF with the vocalization signal was one. d) The LF areas of the V and VN MTFs at a range of intensities for the cell whose RFs and MTFs are shown in a–c. The error bars represent 95% confidence bounds. e) The percent change in LF area evoked by the addition of noise to the vocalization stimuli for a range of overall stimulus intensities for a sample of 8 cells. The error bars represent one standard deviation of the distribution of percent changes in LF area across the sample of cells.
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Related In: Results  -  Collection

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pone-0001655-g005: Context-dependent changes in temporal processing are robust to changes in the overall intensity of the stimulus.a–c) The RFs and MTFs for a typical cell estimated from responses to the V and VN stimuli at overall intensities of 25, 30, and 40 dB SPL above threshold. The preferred frequency of the cell was 10.1 KHz. The error bars represent 95% confidence bounds. The RFs were normalized to have the same peak value for plotting. Before computing the MTFs, RFs were normalized such that the variance of the result of the convolution of the RF with the vocalization signal was one. d) The LF areas of the V and VN MTFs at a range of intensities for the cell whose RFs and MTFs are shown in a–c. The error bars represent 95% confidence bounds. e) The percent change in LF area evoked by the addition of noise to the vocalization stimuli for a range of overall stimulus intensities for a sample of 8 cells. The error bars represent one standard deviation of the distribution of percent changes in LF area across the sample of cells.
Mentions: We also examined the effects of overall stimulus intensity on the observed changes in temporal processing. We estimated temporal RFs from responses to the V and VN stimuli across a range of overall stimulus intensities, as shown for a typical cell at intensities of 25, 30, and 40 dB SPL above threshold in figures 5a–c. The increase in the overall intensity of the stimulus evokes an increase in the LF areas of both the V and VN MTFs, as shown in figure 5d. Accordingly, the magnitude of the decrease in the LF area of the MTF evoked by the addition of noise to the vocalization increased as the overall intensity of the stimulus increased. However, for a sample of 8 cells, the percent decrease in the MTF LF area evoked by the addition of noise remained relatively constant across a range of intensities, as shown in figure 5e. We also found that the observed changes in temporal processing were robust to changes in the spectral properties of the carrier of the vocalization stimulus, as shown in Figure S1.

Bottom Line: We find that the onset of ambient noise evokes a change in receptive field dynamics that corresponds to a change from bandpass to lowpass temporal filtering.We show that these changes occur within a few hundred milliseconds of the onset of the noise and are evident across a range of overall stimulus intensities.Using a simple model, we illustrate how these changes in temporal processing exploit differences in the statistical properties of vocalizations and ambient noises to increase the information in the neural response in a manner consistent with the principles of efficient coding.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology II, Ludwig-Maximilians-University Munich, Martinsried, Germany. lesica@zi.biologie.uni-muenchen.de

ABSTRACT
In this study, we investigate the ability of the mammalian auditory pathway to adapt its strategy for temporal processing under natural stimulus conditions. We derive temporal receptive fields from the responses of neurons in the inferior colliculus to vocalization stimuli with and without additional ambient noise. We find that the onset of ambient noise evokes a change in receptive field dynamics that corresponds to a change from bandpass to lowpass temporal filtering. We show that these changes occur within a few hundred milliseconds of the onset of the noise and are evident across a range of overall stimulus intensities. Using a simple model, we illustrate how these changes in temporal processing exploit differences in the statistical properties of vocalizations and ambient noises to increase the information in the neural response in a manner consistent with the principles of efficient coding.

Show MeSH