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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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Representative examples of the neural response (AN2 neuron from a T. leo) after adaptation to noise stimuli of duration 75 ms (dotted line), 600 ms (dashed line), and 4800 ms (solid line).(A–D) Responses (spike rates) during a test stimulus of 1 s duration (cf. protocol of Figure 3A). Relative intensities of the test stimuli range from −3 dB (A) to +6 dB (D); the average relative intensity of the adapting stimulus was 0 dB. Each stimulus was presented 5 times and the recorded spike trains (1 ms resolution) were convolved with a Gaussian kernel (σ = 50 ms). The instantaneous spike rates were estimated by averaging over the 5 repetitions. The increase of the estimated rate during the first 50 ms is an artifact introduced by filtering the neural response with the Gaussian kernel. Note that the onset latency of the AN2 neuron is in the range of 15 to 18 ms. The spike counts during the sample period (shaded) from 100 ms to 300 ms are used to construct neural response curves.
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pcbi-1000182-g004: Representative examples of the neural response (AN2 neuron from a T. leo) after adaptation to noise stimuli of duration 75 ms (dotted line), 600 ms (dashed line), and 4800 ms (solid line).(A–D) Responses (spike rates) during a test stimulus of 1 s duration (cf. protocol of Figure 3A). Relative intensities of the test stimuli range from −3 dB (A) to +6 dB (D); the average relative intensity of the adapting stimulus was 0 dB. Each stimulus was presented 5 times and the recorded spike trains (1 ms resolution) were convolved with a Gaussian kernel (σ = 50 ms). The instantaneous spike rates were estimated by averaging over the 5 repetitions. The increase of the estimated rate during the first 50 ms is an artifact introduced by filtering the neural response with the Gaussian kernel. Note that the onset latency of the AN2 neuron is in the range of 15 to 18 ms. The spike counts during the sample period (shaded) from 100 ms to 300 ms are used to construct neural response curves.

Mentions: We constructed intensity-response curves to quantify the neural response, as shown in Figure 4 and Figure 5. Therefore, we used the spike count in a 200 ms time window beginning 100 ms after test stimulus onset. The window was chosen such that the influence of the fast adaptation process (time constant of about 40 ms, similar to the one described for the AN1 neuron by Benda and Hennig [21]) is minimized. In the context of this separation of time scales, we are interested only in the coding of slower stimulus dynamics. Hence we consider responses to unmodulated test stimuli and measured spike counts within a 200 ms—rather than a short—time window.


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

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

Representative examples of the neural response (AN2 neuron from a T. leo) after adaptation to noise stimuli of duration 75 ms (dotted line), 600 ms (dashed line), and 4800 ms (solid line).(A–D) Responses (spike rates) during a test stimulus of 1 s duration (cf. protocol of Figure 3A). Relative intensities of the test stimuli range from −3 dB (A) to +6 dB (D); the average relative intensity of the adapting stimulus was 0 dB. Each stimulus was presented 5 times and the recorded spike trains (1 ms resolution) were convolved with a Gaussian kernel (σ = 50 ms). The instantaneous spike rates were estimated by averaging over the 5 repetitions. The increase of the estimated rate during the first 50 ms is an artifact introduced by filtering the neural response with the Gaussian kernel. Note that the onset latency of the AN2 neuron is in the range of 15 to 18 ms. The spike counts during the sample period (shaded) from 100 ms to 300 ms are used to construct neural response curves.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2527132&req=5

pcbi-1000182-g004: Representative examples of the neural response (AN2 neuron from a T. leo) after adaptation to noise stimuli of duration 75 ms (dotted line), 600 ms (dashed line), and 4800 ms (solid line).(A–D) Responses (spike rates) during a test stimulus of 1 s duration (cf. protocol of Figure 3A). Relative intensities of the test stimuli range from −3 dB (A) to +6 dB (D); the average relative intensity of the adapting stimulus was 0 dB. Each stimulus was presented 5 times and the recorded spike trains (1 ms resolution) were convolved with a Gaussian kernel (σ = 50 ms). The instantaneous spike rates were estimated by averaging over the 5 repetitions. The increase of the estimated rate during the first 50 ms is an artifact introduced by filtering the neural response with the Gaussian kernel. Note that the onset latency of the AN2 neuron is in the range of 15 to 18 ms. The spike counts during the sample period (shaded) from 100 ms to 300 ms are used to construct neural response curves.
Mentions: We constructed intensity-response curves to quantify the neural response, as shown in Figure 4 and Figure 5. Therefore, we used the spike count in a 200 ms time window beginning 100 ms after test stimulus onset. The window was chosen such that the influence of the fast adaptation process (time constant of about 40 ms, similar to the one described for the AN1 neuron by Benda and Hennig [21]) is minimized. In the context of this separation of time scales, we are interested only in the coding of slower stimulus dynamics. Hence we consider responses to unmodulated test stimuli and measured spike counts within a 200 ms—rather than a short—time window.

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.

Show MeSH
Related in: MedlinePlus