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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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Actual and predicted responses of auditory neurons to naturalistic stimuli.a) A model of temporal processing in the auditory pathway. The vocalization signal (with or without additive noise) is passed through either the V or VN RF, and the result is fed into an integrate and fire mechanism to generate spikes. b) The temporal RFs estimated from responses to the V (black) and VN (red) stimuli for two cells with preferred frequencies of 12.5 and 3 KHz, respectively. The RFs were normalized to have the same peak value for plotting. c,d) The actual and predicted responses to repeated presentations of the V and VN stimuli for the two cells for which RFs are shown in b. The correlation coefficients between the predicted and actual responses are shown. The correlation coefficients were calculated for responses to novel stimuli (those not used to fit the model) for firing rate in 2 ms bins averaged over 100 repetitions.
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pone-0001655-g006: Actual and predicted responses of auditory neurons to naturalistic stimuli.a) A model of temporal processing in the auditory pathway. The vocalization signal (with or without additive noise) is passed through either the V or VN RF, and the result is fed into an integrate and fire mechanism to generate spikes. b) The temporal RFs estimated from responses to the V (black) and VN (red) stimuli for two cells with preferred frequencies of 12.5 and 3 KHz, respectively. The RFs were normalized to have the same peak value for plotting. c,d) The actual and predicted responses to repeated presentations of the V and VN stimuli for the two cells for which RFs are shown in b. The correlation coefficients between the predicted and actual responses are shown. The correlation coefficients were calculated for responses to novel stimuli (those not used to fit the model) for firing rate in 2 ms bins averaged over 100 repetitions.

Mentions: The principles of efficient coding suggest that adaptive mechanisms should modulate a tradeoff between smoothing (increasing the SNR in the response) and whitening (reducing redundancy), with the optimal balance dependent on the overall SNR of the stimulus [7]. Viewed in this context, the results shown in figure 3 appear to capture the system at the two opposite sides of this tradeoff. Bandpass filtering in the V RF reduces the redundancy of the correlated (1/f) AMs in the vocalization stimulus by whitening at low frequencies, while lowpass filtering in the VN RF increases SNR under noisy conditions by preserving power at low modulation frequencies where the power in the vocalization stimulus is largest. To analyze the relative effectiveness of these two strategies, it is necessary to compare the responses to the vocalization stimulus with and without ambient noise when the system is using each processing strategy. Because of the fast time-course of the changes in temporal processing that we observe, as shown in figure 4, such a comparison cannot be made experimentally. Instead, we use a simple model in which the AMs in the stimulus are passed through either the V or VN RF for a particular cell, and the output of the RF is used to drive a leaky, noisy integrate and fire (IF) spike generator as shown in figure 6a. Figure 6b shows the V and VN RFs for two typical cells, and figures 6c and d show the actual responses of the cells to repeated presentations of the V and VN stimuli, along with the corresponding predicted responses of the model (with the temporal RF matched to the stimulus condition). For the subset of cells for which the model could be cross-validated on responses to novel stimuli (n = 23), the predictions were highly accurate, with correlation coefficients between predicted and actual responses of 0.62±0.09 for the V stimulus and 0.66±0.07 for the VN stimulus (for firing rate in 2 ms bins).


Efficient temporal processing of naturalistic sounds.

Lesica NA, Grothe B - PLoS ONE (2008)

Actual and predicted responses of auditory neurons to naturalistic stimuli.a) A model of temporal processing in the auditory pathway. The vocalization signal (with or without additive noise) is passed through either the V or VN RF, and the result is fed into an integrate and fire mechanism to generate spikes. b) The temporal RFs estimated from responses to the V (black) and VN (red) stimuli for two cells with preferred frequencies of 12.5 and 3 KHz, respectively. The RFs were normalized to have the same peak value for plotting. c,d) The actual and predicted responses to repeated presentations of the V and VN stimuli for the two cells for which RFs are shown in b. The correlation coefficients between the predicted and actual responses are shown. The correlation coefficients were calculated for responses to novel stimuli (those not used to fit the model) for firing rate in 2 ms bins averaged over 100 repetitions.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2249929&req=5

pone-0001655-g006: Actual and predicted responses of auditory neurons to naturalistic stimuli.a) A model of temporal processing in the auditory pathway. The vocalization signal (with or without additive noise) is passed through either the V or VN RF, and the result is fed into an integrate and fire mechanism to generate spikes. b) The temporal RFs estimated from responses to the V (black) and VN (red) stimuli for two cells with preferred frequencies of 12.5 and 3 KHz, respectively. The RFs were normalized to have the same peak value for plotting. c,d) The actual and predicted responses to repeated presentations of the V and VN stimuli for the two cells for which RFs are shown in b. The correlation coefficients between the predicted and actual responses are shown. The correlation coefficients were calculated for responses to novel stimuli (those not used to fit the model) for firing rate in 2 ms bins averaged over 100 repetitions.
Mentions: The principles of efficient coding suggest that adaptive mechanisms should modulate a tradeoff between smoothing (increasing the SNR in the response) and whitening (reducing redundancy), with the optimal balance dependent on the overall SNR of the stimulus [7]. Viewed in this context, the results shown in figure 3 appear to capture the system at the two opposite sides of this tradeoff. Bandpass filtering in the V RF reduces the redundancy of the correlated (1/f) AMs in the vocalization stimulus by whitening at low frequencies, while lowpass filtering in the VN RF increases SNR under noisy conditions by preserving power at low modulation frequencies where the power in the vocalization stimulus is largest. To analyze the relative effectiveness of these two strategies, it is necessary to compare the responses to the vocalization stimulus with and without ambient noise when the system is using each processing strategy. Because of the fast time-course of the changes in temporal processing that we observe, as shown in figure 4, such a comparison cannot be made experimentally. Instead, we use a simple model in which the AMs in the stimulus are passed through either the V or VN RF for a particular cell, and the output of the RF is used to drive a leaky, noisy integrate and fire (IF) spike generator as shown in figure 6a. Figure 6b shows the V and VN RFs for two typical cells, and figures 6c and d show the actual responses of the cells to repeated presentations of the V and VN stimuli, along with the corresponding predicted responses of the model (with the temporal RF matched to the stimulus condition). For the subset of cells for which the model could be cross-validated on responses to novel stimuli (n = 23), the predictions were highly accurate, with correlation coefficients between predicted and actual responses of 0.62±0.09 for the V stimulus and 0.66±0.07 for the VN stimulus (for firing rate in 2 ms bins).

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