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Adaptation and selective information transmission in the cricket auditory neuron AN2.

Wimmer K, Hildebrandt KJ, Hennig RM, Obermayer K - PLoS Comput. Biol. (2008)

Bottom Line: The spike responses were thus reduced for low-intensity sounds.Most remarkably, and in contrast to the infomax principle, adaptation actually reduces the amount of encoded information when considering the whole range of input signals.The response curve changes are also not consistent with the selective coding hypothesis, because the amount of information conveyed about the loudest part of the signal does not increase as predicted but remains nearly constant.

View Article: PubMed Central - PubMed

Affiliation: School of Computer Science and Electrical Engineering, Technische Universität Berlin, Berlin, Germany. klaus@cs.tu-berlin.de

ABSTRACT
Sensory systems adapt their neural code to changes in the sensory environment, often on multiple time scales. Here, we report a new form of adaptation in a first-order auditory interneuron (AN2) of crickets. We characterize the response of the AN2 neuron to amplitude-modulated sound stimuli and find that adaptation shifts the stimulus-response curves toward higher stimulus intensities, with a time constant of 1.5 s for adaptation and recovery. The spike responses were thus reduced for low-intensity sounds. We then address the question whether adaptation leads to an improvement of the signal's representation and compare the experimental results with the predictions of two competing hypotheses: infomax, which predicts that information conveyed about the entire signal range should be maximized, and selective coding, which predicts that "foreground" signals should be enhanced while "background" signals should be selectively suppressed. We test how adaptation changes the input-response curve when presenting signals with two or three peaks in their amplitude distributions, for which selective coding and infomax predict conflicting changes. By means of Bayesian data analysis, we quantify the shifts of the measured response curves and also find a slight reduction of their slopes. These decreases in slopes are smaller, and the absolute response thresholds are higher than those predicted by infomax. Most remarkably, and in contrast to the infomax principle, adaptation actually reduces the amount of encoded information when considering the whole range of input signals. The response curve changes are also not consistent with the selective coding hypothesis, because the amount of information conveyed about the loudest part of the signal does not increase as predicted but remains nearly constant. Less information is transmitted about signals with lower intensity.

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Adaptation induced changes in the mutual information between the stimulus and the neural response.(A1,A2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the whole stimulus range (relative intensity from −4.5 dB to 4.5 dB) and the trimodal amplitude distribution. For each cell the change of the mutual information is calculated as the difference of the mutual information for the ‘trimodal’ (neural response adapted to the trimodal stimulus) and the ‘bimodal’ (neural response adapted to the bimodal stimulus) response curve. The distribution in (A1) is based on the mean values of changes in mutual information for individual cells. (B1,B2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from −4.5 dB to 1.5 dB (including only the two low-intensity peaks of the trimodal stimulus distribution). (C1,C2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from 1.5 dB to 4.5 dB (including only the high-intensity peak of the trimodal stimulus distribution). Triangles denote the median value. The distribution of cells that showed changes that were significant (Bayesian posterior intervals, Methods, Bayesian data analysis) is marked black in (A1,B1,C1). Shaded areas depict the left-tailed 95% posterior intervals in (A2,B2) and the two-tailed 95% posterior interval in (C2).
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pcbi-1000182-g013: Adaptation induced changes in the mutual information between the stimulus and the neural response.(A1,A2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the whole stimulus range (relative intensity from −4.5 dB to 4.5 dB) and the trimodal amplitude distribution. For each cell the change of the mutual information is calculated as the difference of the mutual information for the ‘trimodal’ (neural response adapted to the trimodal stimulus) and the ‘bimodal’ (neural response adapted to the bimodal stimulus) response curve. The distribution in (A1) is based on the mean values of changes in mutual information for individual cells. (B1,B2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from −4.5 dB to 1.5 dB (including only the two low-intensity peaks of the trimodal stimulus distribution). (C1,C2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from 1.5 dB to 4.5 dB (including only the high-intensity peak of the trimodal stimulus distribution). Triangles denote the median value. The distribution of cells that showed changes that were significant (Bayesian posterior intervals, Methods, Bayesian data analysis) is marked black in (A1,B1,C1). Shaded areas depict the left-tailed 95% posterior intervals in (A2,B2) and the two-tailed 95% posterior interval in (C2).

Mentions: For the example neurons in Figure 10, however, we observed a significant decrease in mutual information, varying from a mean value of −0.183 bit (Figure 10A) to −0.372 bit (Figure 10B) and −0.187 bit (Figure 10C). This trend is confirmed by a full analysis of all 20 recorded AN2 cells (Figure 13A), which shows that mutual information decreased for all cells. The median is −0.21 bit (mean: −0.21 bit), and this decrease is significant (the left-tailed 95% posterior interval in Figure 13A2 excludes the value 0 dB). 15 of 20 cells showed an individually statistically significant decrease in mutual information (median −0.24 bit, mean −0.24 bit; black distribution in Figure 13A1). These findings provide strong evidence against the infomax principle.


Adaptation and selective information transmission in the cricket auditory neuron AN2.

Wimmer K, Hildebrandt KJ, Hennig RM, Obermayer K - PLoS Comput. Biol. (2008)

Adaptation induced changes in the mutual information between the stimulus and the neural response.(A1,A2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the whole stimulus range (relative intensity from −4.5 dB to 4.5 dB) and the trimodal amplitude distribution. For each cell the change of the mutual information is calculated as the difference of the mutual information for the ‘trimodal’ (neural response adapted to the trimodal stimulus) and the ‘bimodal’ (neural response adapted to the bimodal stimulus) response curve. The distribution in (A1) is based on the mean values of changes in mutual information for individual cells. (B1,B2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from −4.5 dB to 1.5 dB (including only the two low-intensity peaks of the trimodal stimulus distribution). (C1,C2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from 1.5 dB to 4.5 dB (including only the high-intensity peak of the trimodal stimulus distribution). Triangles denote the median value. The distribution of cells that showed changes that were significant (Bayesian posterior intervals, Methods, Bayesian data analysis) is marked black in (A1,B1,C1). Shaded areas depict the left-tailed 95% posterior intervals in (A2,B2) and the two-tailed 95% posterior interval in (C2).
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pcbi-1000182-g013: Adaptation induced changes in the mutual information between the stimulus and the neural response.(A1,A2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the whole stimulus range (relative intensity from −4.5 dB to 4.5 dB) and the trimodal amplitude distribution. For each cell the change of the mutual information is calculated as the difference of the mutual information for the ‘trimodal’ (neural response adapted to the trimodal stimulus) and the ‘bimodal’ (neural response adapted to the bimodal stimulus) response curve. The distribution in (A1) is based on the mean values of changes in mutual information for individual cells. (B1,B2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from −4.5 dB to 1.5 dB (including only the two low-intensity peaks of the trimodal stimulus distribution). (C1,C2) Distribution and combined posterior density of changes in the transmitted mutual information when considering the stimulus range from 1.5 dB to 4.5 dB (including only the high-intensity peak of the trimodal stimulus distribution). Triangles denote the median value. The distribution of cells that showed changes that were significant (Bayesian posterior intervals, Methods, Bayesian data analysis) is marked black in (A1,B1,C1). Shaded areas depict the left-tailed 95% posterior intervals in (A2,B2) and the two-tailed 95% posterior interval in (C2).
Mentions: For the example neurons in Figure 10, however, we observed a significant decrease in mutual information, varying from a mean value of −0.183 bit (Figure 10A) to −0.372 bit (Figure 10B) and −0.187 bit (Figure 10C). This trend is confirmed by a full analysis of all 20 recorded AN2 cells (Figure 13A), which shows that mutual information decreased for all cells. The median is −0.21 bit (mean: −0.21 bit), and this decrease is significant (the left-tailed 95% posterior interval in Figure 13A2 excludes the value 0 dB). 15 of 20 cells showed an individually statistically significant decrease in mutual information (median −0.24 bit, mean −0.24 bit; black distribution in Figure 13A1). These findings provide strong evidence against the infomax principle.

Bottom Line: The spike responses were thus reduced for low-intensity sounds.Most remarkably, and in contrast to the infomax principle, adaptation actually reduces the amount of encoded information when considering the whole range of input signals.The response curve changes are also not consistent with the selective coding hypothesis, because the amount of information conveyed about the loudest part of the signal does not increase as predicted but remains nearly constant.

View Article: PubMed Central - PubMed

Affiliation: School of Computer Science and Electrical Engineering, Technische Universität Berlin, Berlin, Germany. klaus@cs.tu-berlin.de

ABSTRACT
Sensory systems adapt their neural code to changes in the sensory environment, often on multiple time scales. Here, we report a new form of adaptation in a first-order auditory interneuron (AN2) of crickets. We characterize the response of the AN2 neuron to amplitude-modulated sound stimuli and find that adaptation shifts the stimulus-response curves toward higher stimulus intensities, with a time constant of 1.5 s for adaptation and recovery. The spike responses were thus reduced for low-intensity sounds. We then address the question whether adaptation leads to an improvement of the signal's representation and compare the experimental results with the predictions of two competing hypotheses: infomax, which predicts that information conveyed about the entire signal range should be maximized, and selective coding, which predicts that "foreground" signals should be enhanced while "background" signals should be selectively suppressed. We test how adaptation changes the input-response curve when presenting signals with two or three peaks in their amplitude distributions, for which selective coding and infomax predict conflicting changes. By means of Bayesian data analysis, we quantify the shifts of the measured response curves and also find a slight reduction of their slopes. These decreases in slopes are smaller, and the absolute response thresholds are higher than those predicted by infomax. Most remarkably, and in contrast to the infomax principle, adaptation actually reduces the amount of encoded information when considering the whole range of input signals. The response curve changes are also not consistent with the selective coding hypothesis, because the amount of information conveyed about the loudest part of the signal does not increase as predicted but remains nearly constant. Less information is transmitted about signals with lower intensity.

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Related in: MedlinePlus