Limits...
Neuronal precision and the limits for acoustic signal recognition in a small neuronal network.

Neuhofer D, Stemmler M, Ronacher B - J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. (2010)

Bottom Line: By progressively corrupting the envelope of a female song, we determined the critical degradation level at which males failed to recognize a courtship call in behavioral experiments.At consecutive levels of processing, intrinsic variability increased, while the sensitivity to external noise decreased.We followed two approaches to determine critical degradation levels from spike train dissimilarities, and compared the results with the limits of signal recognition measured in behaving animals.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Humboldt-Universität zu Berlin, Invalidenstrasse 43, 10115, Berlin, Germany. neuhofda@cms.hu-berlin.de

ABSTRACT
Recognition of acoustic signals may be impeded by two factors: extrinsic noise, which degrades sounds before they arrive at the receiver's ears, and intrinsic neuronal noise, which reveals itself in the trial-to-trial variability of the responses to identical sounds. Here we analyzed how these two noise sources affect the recognition of acoustic signals from potential mates in grasshoppers. By progressively corrupting the envelope of a female song, we determined the critical degradation level at which males failed to recognize a courtship call in behavioral experiments. Using the same stimuli, we recorded intracellularly from auditory neurons at three different processing levels, and quantified the corresponding changes in spike train patterns by a spike train metric, which assigns a distance between spike trains. Unexpectedly, for most neurons, intrinsic variability accounted for the main part of the metric distance between spike trains, even at the strongest degradation levels. At consecutive levels of processing, intrinsic variability increased, while the sensitivity to external noise decreased. We followed two approaches to determine critical degradation levels from spike train dissimilarities, and compared the results with the limits of signal recognition measured in behaving animals.

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Influence of signal degradation on spike train dissimilarities. a Mean distances between spike trains in response to the original song and progressively corrupted songs. Ordinate: spike train distances (in arbitrary units); abscissa: degradation level (in dB); ‘orig’ denotes the uncorrupted stimulus. The distance curves are shown for a receptor cell (REC), a local neuron (TN1) and two ascending neurons (AN3, AN6). For each curve representative standard deviations are shown. The value at ‘orig’ corresponds to the ‘intrinsic’ noise (i.e. trial-to-trial variability). b Histogram showing the ratios of the mean distance at 9 dB signal degradation and the mean intrinsic distance. Results of receptor cells, local and ascending neurons are shown as black, gray and open columns (see inset). c Comparison of the trial-to-trial variability (i.e. intrinsic distances for the ‘orig’ stimulus) between processing stages (medians and interquartile ranges; whiskers indicate 10 and 90 percentiles). d The slopes of the distance curves indicate the sensitivity of the neuronal spike pattern to extrinsic noise. N = 13 (REC), 42 (LN) 34 (AN)
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Fig2: Influence of signal degradation on spike train dissimilarities. a Mean distances between spike trains in response to the original song and progressively corrupted songs. Ordinate: spike train distances (in arbitrary units); abscissa: degradation level (in dB); ‘orig’ denotes the uncorrupted stimulus. The distance curves are shown for a receptor cell (REC), a local neuron (TN1) and two ascending neurons (AN3, AN6). For each curve representative standard deviations are shown. The value at ‘orig’ corresponds to the ‘intrinsic’ noise (i.e. trial-to-trial variability). b Histogram showing the ratios of the mean distance at 9 dB signal degradation and the mean intrinsic distance. Results of receptor cells, local and ascending neurons are shown as black, gray and open columns (see inset). c Comparison of the trial-to-trial variability (i.e. intrinsic distances for the ‘orig’ stimulus) between processing stages (medians and interquartile ranges; whiskers indicate 10 and 90 percentiles). d The slopes of the distance curves indicate the sensitivity of the neuronal spike pattern to extrinsic noise. N = 13 (REC), 42 (LN) 34 (AN)

Mentions: As the signal was progressively degraded, the mean distance between spike trains in response to the uncorrupted stimulus (x0) and in response to a degradation level (yi) increased. Figure 2a shows spike train distances for a sample of four neurons (to allow for a comparison between neurons that differed in spike rates, the distances were standardized by the respective mean spike rates). The dramatic change in the envelope of the auditory stimulus seen in Fig. 1a belies the increase in spike train distances, which turned out to be quite modest by comparison. Distances between spike trains in response to the original song and spike trains in response to 9 dB were always lower than those between ‘orig’ spike trains and Poisson spike trains with the same firing rates (not shown). Figure 2b shows the ratios of the mean distance at the highest, 9 dB, signal degradation (y7 in Fig. 1d) and the intrinsic distance for the original song (x0) for receptor cells, local and ascending neurons. For almost all neurons, the spike train distances due to external signal degradation underwent a less than twofold increase relative to the average intrinsic distance (ratio < 2). For many ascending neurons, increasing the external noise led to almost no change in the spike train distances, yielding a distance ratio of close to unity (open columns in Fig. 2b).Fig. 2


Neuronal precision and the limits for acoustic signal recognition in a small neuronal network.

Neuhofer D, Stemmler M, Ronacher B - J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. (2010)

Influence of signal degradation on spike train dissimilarities. a Mean distances between spike trains in response to the original song and progressively corrupted songs. Ordinate: spike train distances (in arbitrary units); abscissa: degradation level (in dB); ‘orig’ denotes the uncorrupted stimulus. The distance curves are shown for a receptor cell (REC), a local neuron (TN1) and two ascending neurons (AN3, AN6). For each curve representative standard deviations are shown. The value at ‘orig’ corresponds to the ‘intrinsic’ noise (i.e. trial-to-trial variability). b Histogram showing the ratios of the mean distance at 9 dB signal degradation and the mean intrinsic distance. Results of receptor cells, local and ascending neurons are shown as black, gray and open columns (see inset). c Comparison of the trial-to-trial variability (i.e. intrinsic distances for the ‘orig’ stimulus) between processing stages (medians and interquartile ranges; whiskers indicate 10 and 90 percentiles). d The slopes of the distance curves indicate the sensitivity of the neuronal spike pattern to extrinsic noise. N = 13 (REC), 42 (LN) 34 (AN)
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Fig2: Influence of signal degradation on spike train dissimilarities. a Mean distances between spike trains in response to the original song and progressively corrupted songs. Ordinate: spike train distances (in arbitrary units); abscissa: degradation level (in dB); ‘orig’ denotes the uncorrupted stimulus. The distance curves are shown for a receptor cell (REC), a local neuron (TN1) and two ascending neurons (AN3, AN6). For each curve representative standard deviations are shown. The value at ‘orig’ corresponds to the ‘intrinsic’ noise (i.e. trial-to-trial variability). b Histogram showing the ratios of the mean distance at 9 dB signal degradation and the mean intrinsic distance. Results of receptor cells, local and ascending neurons are shown as black, gray and open columns (see inset). c Comparison of the trial-to-trial variability (i.e. intrinsic distances for the ‘orig’ stimulus) between processing stages (medians and interquartile ranges; whiskers indicate 10 and 90 percentiles). d The slopes of the distance curves indicate the sensitivity of the neuronal spike pattern to extrinsic noise. N = 13 (REC), 42 (LN) 34 (AN)
Mentions: As the signal was progressively degraded, the mean distance between spike trains in response to the uncorrupted stimulus (x0) and in response to a degradation level (yi) increased. Figure 2a shows spike train distances for a sample of four neurons (to allow for a comparison between neurons that differed in spike rates, the distances were standardized by the respective mean spike rates). The dramatic change in the envelope of the auditory stimulus seen in Fig. 1a belies the increase in spike train distances, which turned out to be quite modest by comparison. Distances between spike trains in response to the original song and spike trains in response to 9 dB were always lower than those between ‘orig’ spike trains and Poisson spike trains with the same firing rates (not shown). Figure 2b shows the ratios of the mean distance at the highest, 9 dB, signal degradation (y7 in Fig. 1d) and the intrinsic distance for the original song (x0) for receptor cells, local and ascending neurons. For almost all neurons, the spike train distances due to external signal degradation underwent a less than twofold increase relative to the average intrinsic distance (ratio < 2). For many ascending neurons, increasing the external noise led to almost no change in the spike train distances, yielding a distance ratio of close to unity (open columns in Fig. 2b).Fig. 2

Bottom Line: By progressively corrupting the envelope of a female song, we determined the critical degradation level at which males failed to recognize a courtship call in behavioral experiments.At consecutive levels of processing, intrinsic variability increased, while the sensitivity to external noise decreased.We followed two approaches to determine critical degradation levels from spike train dissimilarities, and compared the results with the limits of signal recognition measured in behaving animals.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Humboldt-Universität zu Berlin, Invalidenstrasse 43, 10115, Berlin, Germany. neuhofda@cms.hu-berlin.de

ABSTRACT
Recognition of acoustic signals may be impeded by two factors: extrinsic noise, which degrades sounds before they arrive at the receiver's ears, and intrinsic neuronal noise, which reveals itself in the trial-to-trial variability of the responses to identical sounds. Here we analyzed how these two noise sources affect the recognition of acoustic signals from potential mates in grasshoppers. By progressively corrupting the envelope of a female song, we determined the critical degradation level at which males failed to recognize a courtship call in behavioral experiments. Using the same stimuli, we recorded intracellularly from auditory neurons at three different processing levels, and quantified the corresponding changes in spike train patterns by a spike train metric, which assigns a distance between spike trains. Unexpectedly, for most neurons, intrinsic variability accounted for the main part of the metric distance between spike trains, even at the strongest degradation levels. At consecutive levels of processing, intrinsic variability increased, while the sensitivity to external noise decreased. We followed two approaches to determine critical degradation levels from spike train dissimilarities, and compared the results with the limits of signal recognition measured in behaving animals.

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